ISSN 1413-4703 NEOTROPICAL PRIMATES
A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group
Volume 11 N u m b e r 2 August 2003
Editors Anthony B. Rylands Ernesto Rodríguez-Luna
Assistant Editor John M. Aguiar
PSG Chairman Russell A. Mittermeier
PSG Deputy Chairman Anthony B. Rylands Neotropical Primates A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group
Center for Applied Biodiversity Science Conservation International 1919 M St. NW, Suite 600, Washington, DC 20036, USA
ISSN 1413-4703 Abbreviation: Neotrop. Primates
Editors Anthony B. Rylands, Center for Applied Biodiversity Science, Conservation International, Washington, DC Ernesto Rodríguez-Luna, Universidad Veracruzana, Xalapa, México
Assistant Editor John M. Aguiar, Center for Applied Biodiversity Science, Conservation International, Washington, DC
Editorial Board Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK Adelmar F. Coimbra-Filho, Academia Brasileira de Ciências, Rio de Janeiro, Brazil Liliana Cortés-Ortiz, Universidad Veracruzana, Xalapa, México Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA Stephen F. Ferrari, Universidade Federal do Pará, Belém, Brazil Eckhard W. Heymann, Deutsches Primatenzentrum, Göttingen, Germany William R. Konstant, Conservation International, Washington, DC Russell A. Mittermeier, Conservation International, Washington, DC Marta D. Mudry, Universidad de Buenos Aires, Argentina Horácio Schneider, Universidade Federal do Pará, Belém, Brazil Karen B. Strier, University of Wisconsin, Madison, Wisconsin, USA Maria Emília Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Primate Specialist Group Chairman Russell A. Mittermeier Deputy Chair Anthony B. Rylands Co-Vice Chairs for the Neotropical Region Anthony B. Rylands & Ernesto Rodríguez-Luna Vice Chair for Asia Ardith A. Eudey Vice Chair for Africa Thomas M. Butynski Vice Chair for Madagascar Jörg U. Ganzhorn
Design and Layout: Glenda P. Fábregas and Kim Meek, Center for Applied Biodiversity Science, Conservation International, Washington, DC
Editorial Assistance: Liliana Cortés-Ortiz, Universidad Veracruzana, Xalapa, México Mariella Superina, University of New Orleans, Department of Biological Sciences, New Orleans, LA
IUCN/SSC Primate Specialist Group logo courtesy of Stephen D. Nash, 2002.
Front Cover: Photo of a teaching display featuring pygmy marmosets, Cebuella pygmaea, used for environmental education in northeastern Ecuador. Courtesy of Stella de la Torre and Pablo Yépez.
This issue of Neotropical Primates was kindly sponsored by the Margot Marsh Biodiversity Foundation, 432 Walker Road, Great Falls, Virginia 22066, USA, the Houston Zoological Gardens Conservation Program, General Manager Rick Barongi, 1513 North MacGregor, Houston, Texas 77030, USA, and the Los Angeles Zoo, Director John R. Lewis, 5333 Zoo Drive, Los Angeles, California 90027, USA. Neotropical Primates 11(2), August 2003 73
Planning Stage SHORT ARTICLES Our study of five different populations of pygmy marmo- sets in northeastern Ecuador, along with information from ENVIRONMENTAL EDUCATION: A TEACHING TOOL other studies elsewhere, allowed us to summarize several FOR THE CONSERVATION OF PYGMY MARMOSETS aspects of the ecology and behavior of this primate species, (CEBUELLA PYGMAEA) IN THE ECUADORIAN AMAZON such as its habitat preference, feeding behavior, group com- position and parental care. We then recreated this informa- Stella de la Torre tion in a wooden poster of 120 x 90 cm, in which we drew Pablo Yépez a riparian forest, a feeding tree with real holes in the trunk, and the profiles of six animals of different ages and sex Introduction (one reproductive pair, one subadult, one juvenile and two dependent infants), representing a typical group of this spe- The pygmy marmoset (Cebuella pygmaea) is the small- cies. The profiles of these animals were the basis of a puzzle est monkey in the world. It inhabits the upper Amazon of six wooden figures of the six different animals to be at- basin of Ecuador, Colombia, Peru, Bolivia and Brazil tached to the corresponding profiles by the children during (Soini, 1988). In Ecuador, we have records of the species the game (Fig. 1). The wooden poster can be folded up and from about 220 m to 500 m above sea level, in habitats is easily carried. Large sheets of paper, thin cardboard, color along rivers and lakes in the eastern lowlands (de la Torre, pencils, scissors, glue and stickers allowed children to recre- 2000). The habitat specialization of pygmy marmosets ate, in their own drawings, the life of pygmy marmosets makes them particularly vulnerable to anthropogenic im- based on the poster games. pacts, since human settlements and activities are centered on riparian habitats (Meggers, 1989). Thus, despite the Process Stage relatively wide distribution of pygmy marmosets in east- ern Ecuador, we have increasing evidence that this species We carried out this program in two indigenous commu- could be severely disturbed by human activities, altering nities of Ecuadorian Amazonia. The first was the Secoya its social behavior and possibly reducing its population community of Bellavista on the southern bank of the Río size (de la Torre et al., 2000). Aguarico (00°16’42’’S, 76°25’30’’W). The school of this community had 15 children. The second was the Quichua Pygmy marmosets are not included in any of the IUCN categories in the Red Data Book of Ecuadorian mam- mals; they are listed only in the CITES Appendix II (Tirira, 2001). However, based on the evidence we have gathered during almost seven years of research, we suggest that the status of this species needs to be revised. Indeed, the populations we have studied in northeastern Ecuador have been severely affected by live capture, noise pollution and habitat destruction (de la Torre et al., 2000; Yépez et al., 2003). These factors are related to the development of the petroleum industry, the continuous increase of human populations due to high reproductive and migra- tion rates, and the cultural loss which native communities are experiencing due to their rapid insertion into West- ern cultures (Ministerio del Ambiente et al., 2001). All these factors have altered the equilibrium of natural ecosys- tems and are negatively affecting the populations of pygmy marmosets.
Live capture of pygmy marmosets, in particular, is a common practice of children and adults of many indig- enous communities. They are also eaten in some areas, or killed for target practice in others. We believe that these problems could be mitigated with a program of environ- mental education. We began such a program this year, directed to the children of the communities that live close to some of the pygmy marmoset populations we studied. Yépez Pablo Credit: Figure 1. Wooden poster of pygmy marmosets used for teaching The program was based on a didactic game through which games in the schools of the Secoya community of Bellavista (on the children learned about the ecology, behavior and conserva- southern bank of the Río Aguarico), and the Quichua community tion of these small primates. of Añango (on the southern bank of the Río Napo), Ecuador. 74 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 75 community of Añango on the southern bank of the Río mosets in particular, and about the need to maintain and Napo (00°29’29’’S, 76°24’59’’W), with 20 children in its manage wisely the natural resources of the tropical rainfor- school. The ages of the children ranged from 4 to 14 years est. We asked the children to commit to conserve primates old. Our audiences also included 2-5 young adults (ages and their environments. To reinforce this commitment 18-20) and 1-2 older adults (more than 30 years old). We we used happy-face stickers (to make them remember the selected these communities for our pilot work because we benefits of conserving the monkeys and the environment) are studying pygmy marmoset groups living close to these and sad-face stickers (to remember the negative impacts of settlements, and we have evidence that they are continu- disturbing monkeys and the environment) that we stuck on ously affected by live capture and target practice. opposite sides of each child’s face.
In our presentation we first explained to the children the Product Stage purpose of our study of pygmy marmosets. We showed chil- dren some of the equipment we use, such as binoculars and We carried out this environmental education program tape recorders, and showed them how they work. We then between June and August 2003, and thus the long-term began a dialogue to determine what children knew about results are still being analyzed. We have anecdotal evidence pygmy marmosets. We had them answer questions about of the positive effects of the program on the attitude of where pygmy marmosets live, what they eat, how many children of all ages in relation to our work and to pygmy infants are born, how females care for the infants, and how marmosets. After our presentations, children began to ac- humans could affect them. company us on our daily observations, helping us to carry the equipment and to follow and observe the marmosets. After this introduction we began the games with the They also frequently told us that they will not disturb mon- poster. We first asked the children to solve the marmoset keys again and that they wanted us to continue to give our puzzle, pasting each independently moving animal to the presentations in their schools. corresponding profile in the poster (the two dependent infants were not included in this first game). Different We believe that the interactive games we designed with the children pasted each of the four marmoset figures while wooden poster are key to maintaining the attention of chil- we talked about the riparian habitat in which they live. dren. The interest the children of all ages showed in the poster We then told them about the gum-feeding behavior of and their willingness to learn more about pygmy marmosets pygmy marmosets, and let all the children experience how was remarkable. During our presentations all the children and it might feel by licking a vitamin gel that we poured into the accompanying adults were relaxed and frequently laugh- the holes of the “gum tree” on the poster. Children later ing while participating in each of the games. mimicked insect-feeding by finding and eating candies hidden in the classroom. Conclusions
Finally, we talked about the social organization of these These are our first experiences in this community-based primates: the size and composition of groups, the repro- program of environmental education. We are aware of the ductive pattern and some conspicuous infant-caregiver be- need to continue in the communities where we have already haviors (e.g., infant-carrying). We explained to them how worked, and to expand it to other communities in the Ec- important it is for the marmoset infants to be carried and uadorian Amazon. We are currently working on the design attended by other group members, similar to the way that of a more systematic evaluation protocol that will allow human infants need their family to survive. The children us to better analyze the results of the program. Although then participated in a new game with the poster, in which several environmental education programs have been car- we told them that the two infants of the group were lost and ried out in Ecuador, there is still much to do in order to that they were crying for their family. One child partici- improve the environmental awareness of the people in our pated in the game at a time; first we blindfolded the child, country. We hope that our work will help to increase the and then simulated infant crying to guide the blindfolded environmental awareness of Amazonian inhabitants, and to child to the figures of the two infants. Once the child got preserve pygmy marmosets as well as other primate species one of the infants, he or she had to paste it on the back of a and their habitats. caregiver while still blindfolded. Acknowledgements: We thank the children of the Secoya Once this second game was over, children were divided into community of Bellavista and the Quichua community of small groups. Each group was provided with paper, thin Añango for their participation in the program. We thank cardboard, scissors, color pencils and glue, and began to the teachers for allowing us to visit the schools and talk create their own version of a family group of pygmy mar- to the children and for their support during the presenta- mosets in the forest, based on what they learned from the tions. We greatly thank Charles T. Snowdon for his support poster. during all the stages of our work and for his comments on this paper, and Fernanda Tomaselli for her valuable help Our presentation ended with an explanation of the impor- in the fieldwork. We thank the people of Novarum who tance of preserving primates in general and pygmy mar- helped us in the design and construction of the wooden 74 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 75
posters. Our research is supported by NIH Health (Grant 2 R0I MH29775-22). The Ecuadorian Ministry of the Envi- ronment allows us to conduct research in these areas.
Stella de la Torre, Universidad San Francisco de Quito, Av. Interoceánica y Jardines del Este, Cumbayá, Quito, Ecua- dor, e-mail:
References
de la Torre, S. 2000. Primates de la Amazonía Ecuatoriana Figure 1. Recorded wild populations of black lion tamarins – Primates of Amazonian Ecuador. Proyecto PETRAMAZ/ (Leontopithecus chrysopygus). Numbers with circles indicate SIMBIOE, Quito. protected areas. de la Torre, S., Snowdon, C. T. and Bejarano, M. 2000. Effects of human activities on pygmy marmosets in Ecua- dorian Amazonia. Biol. Conserv. 94: 153-163. forest, comprising small forest fragments and gallery forest Meggers, B. J. 1989. Amazonía: Hombre y Cultura en un (440 ha) and a large fragment of 611 ha. Paraíso Ilusorio. Siglo Veintiuno, México. Ministerio del Ambiente, EcoCiencia and Unión Mundial The group was composed of at least five individuals. They para la Naturaleza (UICN). 2001. La Biodiversidad del were calling intensely during the observation period at Ecuador. Informe 2000, C. Josse (ed.). Ministerio del Am- the same time as some bare-throated bellbirds (Procnias biente, EcoCiencia and UICN, Quito. nudicollis). It is possible that the bellbirds were excited by Soini, P. 1988. The pygmy marmoset, genus Cebuella. the presence of the lion tamarins. Foraging associations of In: Ecology and Behavior of Neotropical Primates, Vol. 2, black lion tamarins and insectivorous birds have been de- R. A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho scribed in the literature by Passos (1997), who mentioned and G. A. B. da Fonseca (eds.), pp. 79-129. World Wild- that the birds were sometimes alarmed by the primates. We life Fund, Washington, DC. were able to observe the lion tamarins at heights of 5-8 m Tirira, D. (ed.). 2001. Libro Rojo de Los Mamíferos del Ec- for about 10 minutes, after which they became silent and uador. SIMBIOE/EcoCiencia/Ministerio del Ambiente/ disappeared. No pictures or audio recordings of their vocal- UICN. Serie Libros Rojos del Ecuador, Tomo 1. Pub- izations were taken. licación Especial sobre los Mamíferos del Ecuador 4. Quito. Until recently, black lion tamarins were known to occur in Yépez, P., de la Torre, S., Pallares, M. and Snowdon, C. T. only three protected areas in São Paulo (Morro do Diabo 2002. Área de vida y preferencias alimenticias del leoncillo State Park, Caetetus Ecological Station and Angatuba Eco- Callithrix (Cebuella) pygmaea en el nororiente ecuatoriano. logical Station), and in six other forest fragments located In: CD Memorias del I Congreso de Ecología y Ambiente – Ec- in the western and central regions of the state of São Paulo uador, País Megadiverso, S. de la Torre and G. Reck (eds.). (see Coimbra-Filho, 1970; Coimbra-Filho, 1976; Mamede- Universidad San Francisco de Quito, Ecuador. Costa and Gobbi, 1998; Passos, 1994; Valladares-Pádua and Cullen Jr., 1994; Valladares-Pádua et al., 2002). More recently, two new sub-populations were found in forest frag- THE DISCOVERY OF A NEW POPULATION OF BLACK ments in the eastern part of the state in the municipality of LION TAMARINS (LEONTOPITHECUS CHRYSOPYGUS) Buri (Valladares-Pádua et al., 2002) (Fig. 1). IN THE SERRA DE PARANAPIACABA, SÃO PAULO, BRAZIL This is the eleventh remaining natural population recorded for this species, and the easternmost record of the distribu- Fabio Röhe tion of L. chrysopygus in recent times. Several specimens were André Pinassi Antunes captured by J. Natterer in 1819 and 1822 in the munici- Cristina Farah de Tófoli palities of Cotia and Ipanema, and by E. Garbe in 1902 at Vitoriana; in addition, the pelt of one specimen from Bauru A group of black lion tamarins (Leontopithecus chrysopygus) was given to the São Paulo Zoology Museum (MZSP) by was sighted on 19 December, 2002, at 4:30 pm, at the O. Humel in 1905 (Vieira, 1944; Coimbra-Filho, 1976). Fazenda João XXIII (23°53’09”-23°56’29”S, 47°42’30”- However, none are known to survive in these regions today. 47°40’08”W), in the municipality of Pilar do Sul, state of Because the new Serra de Paranapiacaba population is in a São Paulo, Brazil. The farm belongs to Eucatex S/A and relatively large forest, it may represent a new hope for the is located in the Serra de Paranapiacaba, near the Carlos survival of this species. Surveys and censuses need to be Botelho and Intervales State Parks. The farm is a mosaic carried out in this forest and others in the region, to better of Eucalyptus plantations (1307 ha) and patches of Atlantic determine more exactly the numbers surviving there. 76 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 77
1. Morro do Diabo State Park (Teodoro Sampaio)* conservation of black lion tamarins. In: Lion Tamarins: 2. Fazenda Tucano (Euclides da Cunha Paulista)* and Biology and Conservation, D. G. Kleiman and A. B. Ry- Fazenda Rosanella (Teodoro Sampaio)* lands (eds.), pp.333-351. Smithsonian Institution Press, 3. Fazenda Ponte Branca (Euclides da Cunha Pau- Washington, DC. lista)* Vieira, C. O. 1944. Os símios do estado de São Paulo. Pap. 4. Fazenda Santa Mônica (Teodoro Sampaio)** Avuls. Dept. Zool., São Paulo 4(1): 1-31. 5. Fazenda Santa Maria I (Teodoro Sampaio)** 6. Caetetus Ecological Station (Gália)* 7. Fazenda Rio Claro (Lençois Paulista)* ON THE OCCURRENCE OF THE BLACK LION 8. Fazenda Migrai (Buri)*** TAMARIN (LEONTOPITHECUS CHRYSOPYGUS) IN BURI, 9. Rio Apiaiaçu (Buri)*** SÃO PAULO, BRAZIL 10. Angatuba Ecological Station 11. Fazenda João XXIII (Pilar do Sul) Fernando Silva Lima, Izabel Cristina da Silva Cristiana Saddy Martins, Cláudio Valladares-Pádua *Localities from Valladares-Pádua and Cullen Jr., 1994. **Localities from Valladares-Pádua et al., 2002. The black lion tamarin (Leontopithecus chrysopygus) is ***C. Valladares-Pádua (unpubl.). one of the most endangered of the Neotropical primates (Valladares-Pádua and Cullen, 1994; Rylands and Chi- Acknowledgements: We are grateful to Cláudio Valladares- arello, 2003). Currently, we know of nine locations where Pádua and Eleonore Z. F. Setz for valuable comments and this species occurs, with the largest population – about assistance with the English version of the manuscript, and 820 individuals – occurring in the Morro do Diabo State to Eucatex S/A for logistical support. Park (Valladares-Pádua and Cullen, 1994) in the far west of its range, the Pontal do Paranapanema in the state of São Fabio Röhe, Coordenação de Pesquisas em Ecologia Paulo. Acting on new reports of the occurrence of black (CPEC), Caixa Postal 478, Instituto Nacional de Pesquisas lion tamarins, in July 2003 the NGO IPÊ – Instituto de da Amazônia, Manaus 69011-970, Amazonas, Brazil, e-mail Pesquisas Ecológicas initiated a major programme of sur-
Table 1. Sightings of Leontopithecus chrysopygus in Buri. Fragments were grouped in complexes (1-7, see map). Forest Fragment Area N° of Location Coordinates (complex) (ha) individuals 01 Capão Bonito National Forest (7) 396 Capão Bonito National Forest 2 23°55’14’’S 48°32’45’’W 02 Capão Bonito National Forest (7) 396 Capão Bonito National Forest 2 23°55’14’’S 48°32’45’’W 03 River mouth (6) 83 River mouth (Fazenda Pezzoni) 6 23°55’00’’S 48°32’52’’W Riparian forest on Apiaí-Mirim and Riparian forest, Rios Apiaí-Mirim and 04 504 2 23°49’16’’S 48°34’36’’W Apiaí-Guaçu (5) Apiaí-Guaçu Riparian forest, Rios Apiaí-Mirim Riparian forest, Rios Apiaí-Mirim and 05 504 2-3 23°49’19’’S 48°34’37’’W and Apiaí-Guaçu (5) Apiaí-Guaçu Riparian forest, Rios Apiaí-Mirim Riparian forest, Rios Apiaí-Mirim and 06 504 6-7 23°50’02’’S 48°34’07’’W and Apiaí-Guaçu (5) Apiaí-Guaçu 07 Fazenda Planebrás (2) 273 Fazenda Planebrás 4 23°49’28’’S 48°34’23’’W 08 Riparian forest (4) 20 Riparian forest close to the town of Buri 4 23°42’33’’S 48°39’15’’W 09 River mouth (6) 83 Fazenda Urupês 5 23°47’16’’S 48°35’18’’W 10 River mouth (6) 83 Fernando Espanhol 2 23°49’53’’S 48°33’35’’W 11 Fazenda Floresta (3) 346 Fazenda Floresta 5 23°42’01’’S 48°38’17’’W 12 Fazenda Vale do Apiaí (1) 1007 Fazenda Vale do Apiaí 3 23°39’07’’S 48°34’20’’W Riparian forest, Rios Apiaí-Mirim 13 504 Mata/Estrada 3 23°48’40’’S 48°35’16’’W and Apiaí-Guaçu (5) Riparian forest, Rios Apiaí-Mirim 14 504 Riparian forest 1 23°48’35’’S 48°35’15’’W and Apiaí-Guaçu (5) Riparian Forest, Rios Apiaí-Mirim 15 504 Banks of the Rio Apiaí-Guaçu 4 23°48’59’’S 48°32’47’’W and Apiaí-Guaçu (5) Riparian Forest, Rios Apiaí-Mirim 16 504 Olaria 5 23°50’29’’S 48°35’17’’W and Apiaí-Guaçu (5) Riparian Forest, Rios Apiaí-Mirim 17 504 Olaria 6 23°50’38’’S 48°35’08’’W and Apiaí-Guaçu (5) Riparian Forest, Rios Apiaí-Mirim 18 and Apiaí-Guaçu (5) 504 Olaria 4 23°50’33’’S 48°35’12’’W
References
Coimbra-Filho, A. F. 1976. Os sagüis do gênero Leonto- pithecus Lesson, 1840 (Callithricidae-Primates). Doctoral dissertation, Federal University of Rio de Janeiro, Rio de Janeiro. Rylands, A. B. and Chiarello, A. G. 2003. Official list of Brazilian fauna threatened with extinction – 2003. Neo- trop. Primates 11(1): 43-49. Rylands, A. B., Kierulff, M. C. and Pinto, L. P. 2002. Distribution and status of lion tamarins. In: Lion Tama- rins: Biology and Conservation, D. G. Kleiman and A. B. Rylands (eds.), pp. 42-70. Smithsonian Institution Press, Washington, DC. Valladares-Pádua, C. B., Ballou, J. D., Martins, C. S. and Cullen Jr., L. 2002. Metapopulation management for the conservation of black lion tamarins. In: Lion Tamarins: Biology and Conservation, D. G. Kleiman and A. B. Ry- lands (eds.), pp. 301-314. Smithsonian Institution Press, Washington, DC. Valladares-Pádua, C. B. and Cullen, Jr., L. 1994. Distribu- tion, abundance and minimum viable metapopulation of the black lion tamarin (Leontopithecus chrysopygus). Dodo, J. Wildl. Preserv. Trust 30: 80-88. Valladares-Pádua, C., Prado, F. and Maia, R. G. 2000. Survey of new populations of black-faced lion tamarin Figure 1. Areas of occurrence of Leontopithecus chrysopygus in the (Leontopithecus caissara) in São Paulo and Paraná states. municipality of Buri, São Paulo. 01: Apiaí Valley Farm, 02: Fazenda Instituto de Pesquisas Ecológicas (IPÊ), Nazaré Paulista, Planebrás, 03: Fazenda Floresta, 04: Riparian forest, 05: Riparian forest complex on the Rios Apiaí-Mirim and Apiaí-Guaçu, 06: São Paulo. Unpublished report, Margot Marsh Biodiver- River mouth complex, 07: Capão Bonito National Forest. sity Foundation, Virginia. 78 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 79
sugerem que seu estudo poderia fornecer novas perspectivas DIETA, ÁREA DE VIDA, VOCALIZAÇÕES E sobre o comportamento de emissão de chamados de longo ESTIMATIVAS POPULACIONAIS DE ALOUATTA GUARIBA alcance nos bugios (Oliveira, 2002). EM UM REMANESCENTE FLORESTAL NO NORTE DO ESTADO DO PARANÁ Portanto, pela importância dos fatos mencionados e devido à escassez de dados da região, surgiu o propósito deste tra- Lucas de Moraes Aguiar, Nélio Roberto dos Reis balho, o qual objetivou verificar e analisar a dieta, a área de Gabriela Ludwig, Vlamir José Rocha vida, os percursos diários, as vocalizações de longo alcance (rugido) e as estimativas populacionais da espécie no frag- Introdução mento Mata Doralice.
Na porção sudeste do Brasil, Alouatta guariba (Humboldt, Material e Métodos 1812) é a espécie de bugio característica da Mata Atlântica, limitando sua ocorrência na região do vale do Área de estudo Jequitinhonha, Bahia (Gregorin, 1996), até o município A Mata Doralice situa-se no município de Ibiporã, de São Lourenço do Sul, Rio Grande do Sul (Printes et norte do estado do Paraná, na bacia do Rio Tibagi, mais al., 2001). A subespécie encontrada no Paraná, A. guariba precisamente na região do Baixo Tibagi, nas coordenadas clamitans, possui dicromatismo sexual: Os machos adultos 23°16’S e 51°03’W, a 484 m de altitude. É um fragmento apresentam coloração castanha avermelhada brilhante com florestal de 170 ha, coberto em sua maior parte por uma reflexos dourados, e as fêmeas são de padrão castanho vegetação florestal primária alterada, do tipo Floresta escuro (Auricchio, 1995). Estacional Semidecidual. O fragmento limita-se ao sul com o Rio Tibagi e está circundado por plantios de A situação dessa espécie no estado do Paraná é preocupante. monoculturas, pomares e pastagens (Fig. 1). O solo O estado vem sofrendo intensa devastação principalmente da região é classificado como terra roxa estruturada devido a atividades agrícolas cafeeiras e agropecuárias, que eutrófica e caracteriza-se por ter alta fertilidade natural. dizimam a mata nativa que outrora cobria 84% da área do O clima é subtropical úmido, apresentando as quatro estado (Lange e Jablonski, 1981). De acordo com a SPVS estações bem definidas. A temperatura média anual é de (1996), restam apenas 7% da cobertura vegetal primitiva. 22,45°C e a precipitação média anual é de 114,8 mm. Na região norte, este índice é mais alarmante, uma vez que Os levantamentos fitossociológicos e florísticos realizados a floresta original foi reduzida a valores próximos de 1% por Soares-Silva et al. (1992) e Carmo (1995) apontaram a 2% (Brasil, Paraná, 1987). Assim, são poucos os relatos as famílias vegetais mais representativas como sendo: da presença da espécie na região baixa do Rio Tibagi, onde Meliaceae, Myrtaceae, Fabaceae, Euphorbiaceae, Moraceae provavelmente estão quase extintos. e Mimosaceae, e registraram também a densidade absoluta de 1396 ind./ha, e uma diversidade específica de Os primatas do gênero Alouatta Lacépède, 1799 possuem H’ = 3,6 (I = 0,786). Carmo (1995) verificou que a floresta uma dieta variada, que consiste principalmente de folhas, é constituída por um estrato arbustivo e dois arbóreos, além frutos e outras partes vegetais. Chiarello (1992) afirma que de árvores emergentes com alturas superiores a 20 m. as espécies desse gênero são bastante oportunistas, sendo capazes de sobreviver com dietas compostas basicamente Metodologia por folhas, mas ingerindo os frutos e as flores durante as A coleta de dados foi realizada entre outubro de 2001 e épocas em que estes itens são mais abundantes. Gómez setembro de 2002, através de quatro visitas mensais. O tempo (1999) observa que devido ao fato de as espécies do gênero de acompanhamento dos grupos foi dividido igualmente incluírem uma porção substancial de folhas na sua dieta, para o período matutino e vespertino. Foram acompanhados conseguem sobreviver em fragmentos florestais pequenos diferentemente para cada fim três grupos focais: GI, GII e de até 10 ha. GIII. GI era constituído por um macho adulto dominante, duas fêmeas adultas, um juvenil e um infante; GII por um Um fator determinante no efeito da fragmentação em pri- macho adulto dominante, uma fêmea adulta e um juvenil; e matas é sua área de vida, que possibilita as análises de reque- GIII, por um macho adulto dominante, duas fêmeas adultas, rimentos de áreas para futuras iniciativas de conservação em um juvenil e um infante (classificação etária segundo Mendes fragmentos florestais (Spironello, 2001). Numerosos traba- [1989] e Hirano et al. [1996]). lhos de campo têm avaliado o uso do espaço por diferentes espécies de primatas, contribuindo assim para o esclareci- Dieta: Para quantificar a dieta, os três grupos foram mento da sua ecologia básica (Gómez, 1999). acompanhados utilizando-se o método das freqüências de observação, totalizando 122 h de acompanhamento. Em relação às vocalizações, o gênero Alouatta há muito Na determinação dos itens da dieta foram realizados dois é conhecido como um dos mais notáveis primatas que procedimentos: coleta de fezes e observação direta dos emitem vocalizações de longo alcance. Quanto a isso, A. animais, através do método ad libitum (Altmann, 1974). guariba é uma espécie pouco estudada e algumas evidências, Os itens vegetais não identificados como sementes, frutos, restritas a trabalhos com a subespécie A. g. clamitans, flores e caule foram mencionados como indeterminados 78 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 79
Figura 1. Mapa do Remanescente Florestal Mata Doralice, Ibiporã, PR (170 ha).
(sp. 1, sp. 2, etc.). Foram classificados como “fibras vegetais” Resultados os vestígios de folhas indeterminadas encontradas nas fezes. Para padronizar as amostras fecais e as visuais na somatória Dieta final, considerou-se como uma ocorrência tanto cada espécie Além de Ficus spp., 41 espécies vegetais estiveram presentes vegetal encontrada nas fezes como quanto cada espécie na dieta, identificadas em 21 famílias. Hovenia dulcis foi a ingerida pelo animal na observação direta do grupo focal única espécie exótica utilizada. Moraceae foi a família mais (Rocha, 2001). representativa e freqüente no número de espécies (36,6%). Além das figueiras (23,0%), a base da dieta constituiu- Áreas de vida e percursos diários: Foram estudados dois se de mais 13 espécies vegetais (38,6%), destacando-se grupos vizinhos, GI e GII, acompanhados por 50 e 100 Maclura tinctoria e Sorocea bonplandii, totalizando uma h, respectivamente. A diferença no número de horas de base alimentar de 62,0% (foram consideradas apenas acompanhamento foi porque em GII mensuraram-se os as espécies que obtiveram freqüências acima de 1,0%). percursos diários, assim os resultados de GII podem ser O item “fibras vegetais”, encontrado constantemente nas mais concisos devido ao maior número de amostras. A fezes dos animais, também se apresentou com uma fre- quantificação da área de vida de cada grupo foi feita pelo qüência bastante elevada durante todo o estudo (24,3%) GPS Garmin, modelo eTrex Venture, metodologia adotada (Tabela 1). Quanto aos itens da dieta, registraram-se folhas também por Izar (1999). Os pontos e rotas foram marcados (50,3%), frutos (47,9%), flores (1,4%) e caules (0,3%). pelo aparelho conforme a atividade dos animais, mudanças de direções e possibilidade de contato com satélites dentro Sazonalmente, as espécies vegetais mais consumidas foram: da mata, sendo plotados diariamente em mapas. As áreas frutos de Maclura tinctoria, Ficus spp. e Miconia tristis foram calculadas através do programa AutoCAD 2000. durante a primavera; frutos de Jacaratia spinosa, Phytolacca Os percursos diários foram mensurados no GII pelo GPS dioica e Maclura tinctoria no verão; frutos e folhas de Ficus durante o verão, outono e inverno. spp. durante o outono; e frutos de Pereskia aculeata, Sorocea bonplandii e folhas de Ficus spp. no inverno. Espécies do Vocalizações: Para o estudo sazonal das vocalizações gênero Ficus estavam presentes na dieta durante todas as de longo alcance (loud calls), do tipo rugido, foram estações (Tabela 1), pois os animais consumiram tanto seus cronometrados e anotados os horários, local, sexo e frutos como suas folhas. classe etária do animal, independentemente do grupo emissor. Para a análise contextual, registraram-se somente Durante a primavera e o verão, o consumo de frutos foi le- as emitidas pelos grupos focais da área de vida e de seus vemente mais elevado do que o de folhas (62,3% e 61,0%, vizinhos conhecidos. O método ad libitum foi usado para respectivamente), enquanto que no outono e inverno a o registro dos comportamentos. freqüência alimentar de folhas foi maior (66,0% e 61,0%, respectivamente) (Fig. 2). Notou-se também que durante o Estimativas populacionais: Foi empregado o método outono, o consumo de flores foi maior que nas outras estações da área de vida (Brockelman e Ali, 1987) levando-se e, durante o inverno, houve o consumo de caule de liana. em conta o número médio de indivíduos encontrados por grupo e os resultados das áreas de vida exclusivas e Áreas de vida e percursos diários sobrepostas com grupos vizinhos. Chegou-se, assim, a um Ao final do outono, GI não mais ampliou sua área amos- intervalo de número de grupos, indivíduos e densidade trada, e GII utilizou apenas mais um pequeno trecho na populacional. última estação, o inverno. Ambos os grupos apresenta- 80 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 81
Tabela 1. Espécies vegetais, parte consumida, número de vezes que o item foi consumido durante as estações e freqüência total com que o item participou na dieta de Alouatta guariba. (PC = parte consumida.) Primavera Verãno Outono Inverno Espécies Vegetais PC Total % O N D J F M A M J J A S Fibras vegetais Folhas 6 6 3 10 7 1 1 6 6 11 12 2 71 24,31 Ficus spp. Folhas 2 1 4 3 3 8 2 3 3 6 35 11,99 Ficus spp. Frutos 7 1 2 4 4 4 2 5 3 32 10,96 Maclura tinctoria Frutos 5 7 4 2 3 2 23 7,88 Sorocea bonplandii Frutos 3 1 10 1 15 5,14 Pereskia aculeata Frutos 3 7 5 15 5,14 Jacaratia spinosa Frutos 5 6 11 3,77 Phytolacca dioica Frutos 8 8 2,74 Pisonia ambigua Folhas 1 3 1 1 6 2,05 Miconia tristis Frutos 1 5 6 2,05 sp. 5 Frutos 7 7 2,39 Lauraceae Frutos 4 4 1,37 Syagrus romanzoffianum Frutos 3 1 4 1,37 Casearia sp. Folhas 1 1 2 4 1,37 Rollinia sericea Frutos 3 3 1,03 Jacaratia spinosa Folhas 2 1 3 1,03 Aspidosperma polyneuron Folhas 2 1 3 1,03 Outros (33 Itens) 14,28 Total 24 23 14 52 32 3 12 22 23 33 38 16 292 100%
ram áreas bem definidas. Ao final das estações, o maior grupo, GI, com cinco indivíduos, explorou a maior área (6 ha), com área nuclear de 1,5 ha, e o menor grupo, GII, com três indivíduos, explorou 5 ha, com área nuclear de 1,6 ha (Fig. 3). A exigência espacial dos grupos resultou em média de 1,45 ha/ind. GII deteve quatro figueiras adultas (Ficus spp.) em sua área nuclear e GI deteve apenas duas, as mesmas foram bastante utilizadas como árvores de dor- mida dos grupos.
Os grupos utilizaram diferentes tamanhos e setores de Figura 2. Freqüência dos itens alimentares nas estações: Primavera de 2001 e verão, outono e inverno de 2002. área ao longo das estações (Fig. 4). As áreas foram usadas de modo homogêneo na primavera e verão e heterogêneo no outono e inverno, sendo que nestas duas últimas es- tações foi maior a utilização de sub-áreas pelos animais, as quais foram influenciadas principalmente por Ficus spp. GI obteve maior área na primavera (3,5 ha) e verão (3,7 ha), reduzindo-a em quase um hectare no outono (2,7 ha) e inverno (2,4 ha). Já GII manteve um tamanho quase constante, em média 2,4 ha ao longo das estações. Os dois grupos restringiram suas atividades a locais próximos às suas áreas nucleares no inverno, e alimen- taram-se quase que exclusivamente de frutos de Sorocea bonplandii e folhas de Ficus spp. No verão, registrou-se a única sobreposição de área entre os grupos focais (0,21 ha) (Fig. 4b).
Os percursos diários, medidos no GII, tiveram média de 280 m/dia (n = 7), variando entre 120 m/dia a 500 m/dia. Os maiores valores foram medidos no verão (média = 367 m/dia) e os menores no inverno (média = 200 m/dia), Figura 3. Áreas de vida dos grupos focais: GI, 6 ha com área tendo-se registrado também nesta estação o menor percur- nuclear de 1,5 ha e GII, 5 ha com área nuclear de 1,6 ha. so, 120 m/dia. 80 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 81
Figura 4. Variação sazonal no uso de diferentes setores da área de vida dos grupos focais: a) Primavera, GI: 3,5 ha e GII: 2,2 ha; b) Verão, GI: 3,7 ha e GII: 2,6 ha; c) Outono, GI: 2,7 ha e GII: 2,5 ha; d) Inverno, GI: 2,4 ha e GII: 2,4 ha.
Vocalizações registrada na área nuclear do GI. Houve apenas um registro De todas as vocalizações de longo alcance do tipo rugido de encontro intergrupal, resultando em vocalizações pelos registradas (n = 19), 74% foi no período da tarde com grupos conflitantes. O número de vocalizações dos grupos um pico das 15 às 17 h. Não houve registro do pico de focais relacionou-se ao número de vizinhos transgressores vocalização no alvorecer (dawn chorus). Os rugidos foram identificados, bem como a porcentagem de sobreposições contínuos e duravam em média 13 min, sendo na maioria de suas áreas: GI – 10 vocalizações / 3 grupos vizinhos e 1 das vezes executados apenas pelo macho adulto dominante macho adulto solitário transgressor, 30% de área sobreposta; (84% dos registros). Em uma ocasião, a fêmea vocalizou GII – 1 vocalização / 1 grupo vizinho e 1 macho subadulto junto com o macho dominante do grupo, e em outra, a fêmea solitário transgressor, 10% de área sobreposta. vocalizou sozinha ao lado do macho dominante. Um macho de hierarquia inferior vocalizou apenas em um registro. Estimativas populacionais Sazonalmente, 42% das vocalizações foram registradas no Distinguiu-se no total pelo menos seis grupos diferentes e verão, seguidas de 26% no outono, 16% na primavera e três machos solitários. O maior grupo continha seis indiví- 16% no inverno. As vocalizações de GI e vizinhos ocorreram duos e o menor três. Com exceção de um grupo que pos- próximas aos limites de suas áreas, em regiões periféricas, suía mais de um macho adulto (justamente o maior grupo), na direção de outros grupos. Somente uma vocalização foi todos apresentavam-se com um macho adulto dominante, 82 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 83 suas fêmeas e indivíduos juvenis. Em média foi constatado relacionados diretamente às duas estratégias adaptativas 4,5 indivíduos por grupo. de maximização de energia, uma de alto-custo, alta-recom- pensa e outra de baixo-custo, baixa-recompensa (Zunino, Com os resultados das áreas de vida dos grupos focais e com 1986), conforme as mudanças das fases fenológicas das a média de indivíduos por grupo, foi estimada em média a espécies que compõem a dieta. população de A. guariba. Poderia haver de 31 a 39 grupos habitando a mata durante o período de estudo, totalizando A freqüência total com que os frutos foram utilizados está de 140 a 175 indivíduos, com uma densidade populacional acima das estimativas observadas para o gênero. Entre as de 0,82 a 1,02 indivíduos/ha. espécies de Alouatta, somente nos trabalhos com A. seniculus e A. palliata (ver tabela comparativa em Hirano, 1996) Discussão verificaram-se resultados onde ocorre uma equivalência de ambos os itens consumidos ou onde o consumo do Dieta item fruto foi superior ao item folha, corroborando com o O gênero Alouatta é bastante seletivo, parecendo ter fortes presente trabalho. preferências por algumas espécies vegetais e até mesmo por certos indivíduos dentro de algumas espécies particulares Áreas de vida e percursos diários (Milton, 1977; Sussman, 2000). Estudos com A. guariba O tamanho das áreas de vida aqui mensuradas (6 e 5 ha) demonstraram uma marcante seletividade alimentar: Chia- estão de acordo com as pequenas áreas citadas para as rello (1992) verificou que mais da metade da dieta destes espécies de Alouatta, o que provavelmente ocorra devido animais (54,5%) provém de apenas seis espécies; Limeira ao reflexo do comportamento folívoro alimentar visto em (1997) citou apenas duas como base da dieta, representan- todo gênero. Primatas folívoros têm áreas de vida menores do 55%; e Jardim e Oliveira (2000) relataram a importân- que os frugívoros e onívoros (Milton e May, 1976; Fleagle, cia de cinco espécies para estes bugios, constituindo 70% 1999). As dimensões aqui verificadas podem estar próximas de freqüência total. Na Mata Doralice, a base da dieta dos tamanhos reais já que GI não explorou novas áreas no constituiu-se de um número maior de espécies, Ficus spp. outono e inverno, e GII explorou apenas um pequeno novo e 13 outras (62%), demonstrando uma menor seletividade setor na última estação de coleta, o inverno. Em comparação quando comparada a outros trabalhos. aos trabalhos com a espécie A. guariba, estas áreas foram menores que as encontradas por Mendes (1989) (7,94 ha), Moraceae foi a família mais freqüente (36,6%) sendo as Gaspar (1997) (8,5 ha) e Limeira (2000) (11,6 ha), mas espécies de Ficus as mais presentes na dieta, consumidas próximas às de Chiarello (1992) (4,1 ha). Tal semelhança durante todas as estações de estudo. As figueiras são uma ocorreu apesar do número de indivíduos e grau de folivoria fonte alimentar importante para muitas espécies de prima- serem maiores e o grau de frugivoria ser menor em relação tas, inclusive para Alouatta (ver Terborgh, 1986; Young, aos verificados neste trabalho, evidenciando diferenças nas 1983; Sussman, 2000; Rocha, 2001). No outono, quando estratégias utilizadas pela mesma espécie em diferentes a disponibilidade dos frutos parece ser menor, as figueiras habitats. Spironello (2001) sugeriu que diferenças ecológicas foram importantes tanto no consumo de frutos como de entre as áreas de estudo podem resultar em grandes folhas: Fato também observado por Prates (1990) que con- diferenças no requerimento de área pela mesma espécie ao siderou o gênero Ficus como sendo a base da alimentação longo de sua distribuição geográfica. Ainda, Crockett and deste primata. Figueiras e outras espécies da família também Eisenberg (1987) sugerem que as diferenças de tamanho nas mostraram-se importantes para outras espécies de Alouatta: áreas de vida estão mais associadas às diferenças ambientais. A. palliata (Milton, 1977; Solano et al., 1999); A. pigra O número de indivíduos por grupo foi outro fator que (Schlichte, 1978); A. caraya (Marques e Marques, 1995) e influenciou o tamanho das áreas de vida, pois GI (5 A. seniculus (Palacios e Rodriguez, 2001). indivíduos) utilizou 1 ha a mais do que GII (3 indivíduos), concordando com Strier (1987). A maior procura por O freqüente uso de folhas como fonte de proteínas (Braza figueiras adultas por GI também poderia ter aumentado sua et al., 1983; Torres de Assumpção, 1986) e frutos como área em comparação a GII, já que aquele apresentou menor fonte de carboidratos não estruturais (Smith, 1977) de número destas árvores em sua área nuclear, utilizando sua diversas espécies pode ser explicada pela necessidade de área de vida de modo mais homogêneo. uma dieta nutricionalmente balanceada, sendo que Milton (1980) considera comportamentais as adaptações para a Sazonalmente, os grupos utilizaram suas áreas em diferentes folivoria neste gênero. setores conforme a distribuição espácio-temporal de frutos e folhas. As estratégias citadas por Zunino (1986) pareceram No total, a porcentagem de folhas e frutos consumidos foi ser utilizadas pelos animais. GI apresentou maiores semelhante. Entretanto, notou-se uma diferença sazonal, áreas na primavera e verão, período de maior frugivoria, visto que o consumo de frutos em períodos de abundância que coincidiu com a frutificação de Maclura tinctoria (primavera e verão) foi maior em relação aos períodos de e Jacaratia spinosa, respectivamente. Di Bitetti (2001) escassez (outono e inverno) quando houve aumento no também verificou um aumento da área de vida de Cebus consumo de folhas e flores. Bicca-Marques (1991) atribuiu apella que coincidiu com a frutificação de quatro árvores de essas diferenças às ofertas sazonais de determinados itens M. tinctoria. A procura pelos frutos de J. spinosa foi o 82 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 83
principal fator responsável pela sobreposição registrada longo alcance atuava basicamente como um mecanismo de entre GI e GII e também responsável pela maior área espaçamento entre os grupos em uma espécie não-territorial. sazonal de GI, já que esta espécie arbórea apresentou um Na segunda, foi proposto um contexto de competição baixo Índice de Valor de Importância nos levantamentos sexual, onde os rugidos atuariam mais como um meio de florísticos e é uma espécie que ocorre em baixas densidades evitar o acesso às fêmeas por machos externos ao grupo, mas (Lorenzi, 2000). No outono e inverno, GI diminuiu o posteriormente reconheceu-se que esse comportamento tamanho de sua área em 20%, coincidindo com o período pode desempenhar um papel na defesa de outros recursos de maior índice de folivoria. No inverno, a utilização de (Sekulic, 1983). Neste trabalho, não foi detectado um coro Ficus spp. e Sorocea bonplandii na área nuclear do grupo matinal, o que constitui uma característica da espécie, como contribuiu para a redução da área, já que esta espécie também verificado por Mendes (1989), Chiarello (1995) e arbórea apresenta alta freqüência e Índice de Valor de Oliveira (2002). Importância (Soares-Silva et al., 1992). Apesar do tamanho da área de vida de GII não apresentar variações sazonais, os Os grupos de A. guariba pareceram ser territoriais, maiores percursos foram medidos no verão e os menores conforme constatado também por Mendes (1989) e Hirano no inverno, o que poderia ser um reflexo das estratégias et al. (1996). No que diz respeito à defesa de suas áreas bem citadas por Zunino (1986). definidas, suas vocalizações foram emitidas principalmente nas periferias, como assinalou Mendes (1989), e na direção A riqueza de figueiras no fragmento, evidenciada pelos de seus vizinhos. Além disso, verificou-se que o grupo com trabalhos de levantamento florístico, poderia sustentar as maior número de vizinhos e maior porcentagem de área diferenças no tamanho e no modo de uso da área quando sobreposta (GI) vocalizou dez vezes mais do que o grupo com comparados a outros trabalhos, já que foi nítida a influência menor número de vizinhos e menor porcentagem de área destas, principalmente em épocas de escassez de alimentos. sobreposta (GII), parecendo ter sofrido maior quantidade No outono houve a procura por figueiras em frutificação de estímulos para a emissão deste comportamento. Mitani e no inverno a procura por folhas novas. Neville et al. e Rodman (1979) ressaltaram que em primatas, a defesa (1988) destacam que o uso de área de Alouatta é relatado territorial é funcionalmente dependente da procura por diretamente para a distribuição de fontes preferidas de fontes de comida dentro de uma pequena área de vida, comida, particularmente Ficus. e que estes animais defenderão uma área somente se seus regimes alimentares permitirem. Assim, as pequenas áreas Para Alouatta, os percursos diários estão relacionados à de vida dos grupos focais e um alto índice de frugivoria qualidade do habitat e são também adaptações relacionadas visto neste trabalho apontam para o fato de que estes à dieta folívora utilizada (Bicca-Marques e Calegaro- animais, bem como suas vocalizações, possivelmente estão Marques, 1995). Em relação aos percursos de GII, estes inseridas no contexto de territorialidade, com a função de estão próximos aos pequenos percursos encontrados para defesa de espaço. o gênero, porém aqui verificaram-se menores médias. Mais uma vez as diferenças verificadas poderiam mostrar, além Sazonalmente, a maior porcentagem de vocalizações foi de diferentes tamanhos grupais, diferentes estratégias em registrada no verão, período que correspondeu ao maior resposta às disponibilidades de alimento. registro de sobreposições de áreas entre GI e GII, e desse com outros grupos invasores. O outono foi a estação com Vocalizações o segundo maior registro, apresentando uma maior procura Os rugidos na Mata Doralice apresentaram-se contínuos, por Ficus spp. em frutificação. Ambos os casos podem ter diferindo de outras espécies como A. palliata e A. seniculus colocado os grupos vizinhos em maior probabilidade de (Oliveira, 2002). O número registrado (n = 19) foi inferior encontros entre si, podendo levá-los a situações de disputa. aos trabalhos de Mendes (1989), Chiarello (1995) e Em contrapartida, registrou-se a menor porcentagem de Oliveira (2002). Isto provavelmente está relacionado a vocalizações no inverno, período em que os animais restrin- um baixo número de encontros intergrupais presenciados giram mais suas atividades às áreas nucleares. e a uma menor porcentagem de sobreposições de áreas verificadas entre os grupos, resultantes de uma densidade Estimativas populacionais não alta. Gaspar (veja Oliveira, 2002), também verificou As estimativas registradas para a espécie (0,82 ind/ha a um número baixo de vocalizações (n = 17) em uma área de 1,02 ind/ha) partiram da hipótese de a Mata Doralice baixa densidade da espécie. ser homogênea e chegou-se a resultados inferiores, se comparados aos trabalhos de Mendes (1989) e Chiarello O pico de vocalização encontrado na Mata Doralice (entre (1992), porém superiores em comparação com as baixas 15 e 17 h) está muito próximo ao encontrado por Mendes densidades encontradas por Pinto et al. (1993). Todavia, (1989) e ao pico vespertino encontrado por Chiarello é importante salientar que esta densidade pode sofrer (1995). Muitos autores detectaram a presença do coro alterações se considerar a heterogeneidade da mata, uma matinal em algumas espécies de Alouatta, tais como em A. vez que os grupos foram estudados numa área de floresta palliata (Carpenter, 1934; Whitehead, 1987, 1989) e A. primária e o fragmento também compreende um trecho seniculus (Sekulic, 1982). Na primeira espécie, os autores de floresta secundária. As densidades populacionais apoiaram a idéia de que o contexto das vocalizações de encontradas na Mata Doralice podem estar sofrendo pressão 84 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 85 de caça, mesmo que baixa, mas que ainda é existente neste Brockelman, W. e Ali, R. 1987. Methods for surveying fragmento. Vale ressaltar que no Parque Estadual Mata dos and sampling forest primate populations. Em: Primate Godoy (o fragmento florestal mais representativo da região Conservation in the Tropical Rain Forest, C. W. Marsh e R. do Baixo Tibagi, com 680 ha), a espécie A. guariba está A. Mittermeier (eds.), pp.23-62. Alan R. Liss, New York. extinta, provavelmente devido à caça predatória (Peracchi Carmo, M. R. B. 1995. Levantamento florístico e fitosso- et al., 2002). ciológico do remanescente florestal da Fazenda Doralice, Ibiporã, PR. Monografia de Bacharelado, Universidade Conclusões Estadual de Londrina, Londrina. Carpenter, C. R. 1934. A field study of the behavior and Diante de todo o exposto, concluiu-se que há uma grande social relations of howling monkeys. Comp. Psychol. necessidade da manutenção da Mata Doralice, e outros Monog. 10: 1-168. fragmentos afins, para aplicação de projetos de manejo, Chiarello, A. G. 1992. Dieta, padrão de atividade e área de enriquecimento ambiental e genético para esta população vida de um grupo de bugios (Alouatta fusca), na reserva de isolada de bugios, já que este fragmento é um dos poucos Santa Genebra. Dissertação de Mestrado, Universidade relatos da presença da espécie na região baixa da bacia do Estadual de Campinas, Campinas. Rio Tibagi, onde provavelmente estão quase extintos. Não Chiarello, A. G. 1995. Role of loud calls in brown howlers, obstante, salienta-se a importância da criação de corredores Alouatta fusca. Am. J. Primatol. 36: 213-222. para o estabelecimento de metapopulações para A. guariba Crockett, C. M. e Eisenberg, J. F. 1987. Howlers: Variations na região. in group size and demography. Em: Primate Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrang- Agradecimentos: Ao proprietário da Fazenda Doralice, ham e T. T. Struhsaker (eds.), pp.54-68. The University Sr. Pedro Favoreto, e a todos os moradores locais. Ao of Chicago Press, Chicago. engenheiro, Sr. João Aristides de Aguiar, ao Prof. Anselmo Di Bitetti, M. S. 2001. Home range use by the tufted ca- Ludwig e aos biólogos Isaac Passos de Lima, José Marcelo puchin monkey (Cebus apella nigritus) in a subtropical Domingues Torezan, Manoel Ronaldo Carvalho Paiva e rainforest of Argentina. J. Zool., Lond. 253: 33-45. Edmilson Bianchini. Fleagle, J. G. 1999. Primate Adaptation and Evolution. 2o Edição. Academic Press, New York. Lucas de Moraes Aguiar, Rua Bronislau Ostoja Roguski Gaspar, D. A. 1997. Ecology and behavior of the brown 649, Casa 3, Bairro Jardim das Américas, Curitiba 81540- howling monkey, Alouatta fusca. Neotrop. Primates 5(3): 080, Paraná, Brasil, Nélio Roberto dos Reis, Laboratório 80-81. de Ecologia, Departamento de Biologia Animal e Vegetal, Gómez, A. M. S. 1999. Ecologia e comportamento de Universidade Estadual de Londrina, Caixa Postal 6001, Alouatta seniculus em uma mata de terra firme na Ama- Londrina 86051-990, Paraná, Brasil, Gabriela Ludwig, zônia Central. Dissertação de Mestrado, Universidade Rua Bronislau Ostoja Roguski 649, Casa 3, Bairro Jardim Federal de Minas Gerais, Belo Horizonte. das Américas, Curitiba 81540-080, Paraná, Brasil, e Vlamir Gregorin, R. 1996. Variação geográfica e taxonomia das José Rocha, Klabin S. A., Klabin Florestal PR, Manejo espécies brasileiras do gênero Alouatta Lacépède, 1799 Ambiental, Fazenda Monte Alegre, Lagoa s/no. – Pesquisa (Primates, Atelidae). Dissertação de Mestrado, Universi- Florestal, Lagoa 84279-000, Paraná, Brasil. E-mail: dade de São Paulo, São Paulo.
Limeira, V. L. A. G. 2000. Uso do espaço por um grupo Schlichte, H. J. 1978. A preliminary report on the habitat de Alouatta fusca clamitans em um fragmento degradado utilization of a group of howler monkeys (Alouatta de Floresta Atlântica. Em: A Primatologia no Brasil – 7, villosa pigra) in the National Park of Tikal, Guatemala. C. Alonso e A. Langguth (eds.), pp.181-196. Sociedade Em: The Ecology of Arboreal Folivores, G. G. Montgom- Brasileira de Primatologia, João Pessoa. ery (ed.), pp.551-559. Smithsonian Institution Press, Lorenzi, H. 2000. Árvores Brasileiras: Manual de Identifi- Washington, DC. cação e Cultivo de Plantas Arbóreas Nativas do Brasil. 3a Sekulic, R. 1982. The function of howling in red howler Edição. 2 volumes. Instituto Plantarum, São Paulo. monkeys (Alouatta seniculus). Behaviour 81: 38-54. Mendes, S. L. 1989. Estudo ecológico de Alouatta fusca Sekulic, R. 1983. The effect of female calls on male howling (Primates: Cebidae) na Estação Biológica de Caratinga, in red howler monkeys (Alouatta seniculus). Int. J. Prima- MG. Revista Nordestina de Biologia 6: 71-104. tol. 4: 291-305. Milton, K. 1977. The foraging strategy of the howler Smith, C. C. 1977. Feeding behavior and social organization monkey Alouatta palliata in the tropical forest of Barro in howler monkeys. Em: Primate Ecology, T. H. Clutton- Colorado Island, Panama. Tese de Doutorado, New York Brock (ed.), pp.97-126. Academic Press, London. University, New York. Soares-Silva, L. H., Bianchini, E., Fonseca, E. P., Dias, M. Milton, K. 1980. The Foraging Strategy of Howler Monkeys: C., Medri, M. E. e Zangaro Filho, W. 1992. Composição A Study In Primate Economics. Columbia University Press, florística e fitossociologia do componente arbóreo das New York. florestas ciliares da bacia do Rio Tibagi. 1. Fazenda Milton, K. e May, M. L. 1976. Body weight, diet and home Doralice – Ibiporã, PR. Revta. Inst. Florest., Curitiba 4(1): range area in primates. Nature, Lond. 259: 459-462. 199-206. Mitani, C. e Rodman, P. S. 1979. Territoriality: The rela- Solano, S. J., Martínez, T. J. O., Estrada, A. e Coates- tion of ranking pattern and home range size to defenda- Estrada, R. 1999. Uso de plantas como alimento por bility, an analysis of territoriality among primate species. Alouatta palliata en un fragmento de selva en Los Tuxtlas, Behav. Ecol. Sociobiol. 5: 241-251. México. Neotrop. Primates 7(1): 8-11. Neville, M. K., Glander, K. E., Braza, F. e Rylands, A. B. Spironello, W. R. 2001. The brown capuchin monkey 1988. The howling monkeys, genus Alouatta. Em: Eco- (Cebus apella): Ecology and home range requirements logy and Behavior of Neotropical Primates, Vol. 2, R. A. in Central Amazonia. Em: Lessons from Amazonia: Mittermeier, A. B. Rylands, A. F. Coimbra-Filho e G. A. The Ecology and Conservation of a Fragmented Forest, B. da Fonseca (eds.), pp.349-453. World Wildlife Fund, R. O. Bierregaard, Jr., C. Gascon, T. E. Lovejoy e Washington, DC. R. Mesquita (eds.), pp.271-283. Yale University Press, Oliveira, D. A. G. 2002. Vocalizações de longo alcance de New Haven. Alouatta fusca clamitans e Alouatta belzebul belzebul: Es- SPVS. 1996. Manual para Recuperação da Reserva Florestal trutura e contextos. Tese de Doutorado, Universidade de Legal. Sociedade de Pesquisa em Vida Selvagem e Educa- São Paulo, São Paulo. ção Ambiental (SPVS), Curitiba. Palacios, E. e Rodriguez, A. 2001. Ranging pattern and Strier, K. B. 1987. Ranging behavior of woolly spider use of space in a group of red howler monkeys (Alouatta monkeys or muriquis (Brachyteles arachnoides). Int. J. seniculus) in a southeastern Colombian rainforest. Am. J. Primatol. 8: 575-591. Primatol. 55: 233-251. Sussman, R. W. 2000. Primate Ecology and Social Structure, Peracchi, A. L., Rocha, V. R. e Reis, N. R. 2002. Vol. 2: New World Monkeys. Pearson Custom Publishing, Mamíferos não voadores da bacia do Rio Tibagi. Em: Needham Heights, MA. A Bacia do Rio Tibagi, M. E. Medri, E. Bianchini, Terborgh, J. 1986. Keystone plant resources in the tropical O. A. Shibatta e J. A. Pimenta (eds.), pp.225-249. Editora rainforest. Em: Conservation Biology: Science of Scarcity MC Gráfica, Londrina, Paraná. and Diversity, M. E. Soulé (ed.), pp.330-344. Sinauer Pinto, L. P. S., Costa, C. M. R., Strier, K. B. e Fonseca, G. Associates, Sunderland, MA. A. B. 1993. Habitat, density and group size of primates in Torres de Assumpção, C. 1986. The behaviour and ecology a Brazilian tropical forest. Folia Primatol. 61: 135-143. of the primates in southeastern Brazil, with a reappraisal Prates, J. C., Gayer, S. M. P., Kunz Jr., L. F. e Buss, G. 1990. of Cebus apella races. Tese de Doutorado, University of Feeding habits of the brown howler monkey Alouatta Edinburgh, Edinburgh. fusca clamitans (Cabrera, 1940) (Cebidae, Alouattinae) in Whitehead, J. M. 1987. Vocally mediated reciprocity the Itapuã State Park: A preliminary report. Acta Biologica between neighbouring groups of mantled howling Leopoldensia 12: 175-188. monkeys, Alouatta palliata palliata. Anim. Behav. 35: Printes, R. C., Liesenfeld, M. V. A. e Jerusalinsky, L. 2001. 1615-1627. Alouatta guariba clamitans Cabrera, 1940: A new south- Whitehead, J. M. 1989. Acoustic correlates of internal ern limit for the species and for Neotropical primates. states in free-ranging primates: The example of the Neotrop. Primates 9(3): 118-121. mantled howling monkey, Alouatta palliata. Em: Current Rocha, V. J. 2001. Ecologia de mamíferos de médio e Primatology, Volume 2: Social Development, Learning and grande portes do Parque Estadual Mata dos Godoy, Behaviour, J. J. Roeder, B. Thierry, J. R. Anderson e N. Londrina, Paraná. Tese de Doutorado, Universidade Herrenschmidt (eds.), pp.221-226. Université Louis Federal do Paraná, Curitiba. Pasteur, Strasbourg. 86 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 87
Young, A. L. 1983. Preliminary observations on the ecol- 1000 m. It is diurnal and lives in groups of seven to nine ogy and behavior of the muriqui and brown howler individuals, although group sizes of up to 17 have been re- monkey. Tese de Bacharelado, Harvard University, ported (Bicca-Marques, 1992). Leaves and fruits comprise Cambridge, MA. the majority of its diet. Although not directly threatened, Zunino, G. E. 1986. Algunos aspectos de la ecología y A. caraya suffers from the severe and ongoing fragmentation etología del mono aullador negro (Alouatta caraya) en of its habitat in the Cerrado. In this context it is critical to habitats fragmentados. Tese de Doutorado, Facultad de identify new sites where it may occur, each of which will be Ciencias Exatas y Naturales de la Universidad de Buenos important to the long-term survival of this species. Aires, Buenos Aires. In this report, we register the occurrence of Callithrix geoffroyi and Alouatta caraya in a small fragment of Atlantic CALLITHRIX GEOFFROYI (PRIMATES: CALLITRICHIDAE) forest on the eastern border of the Serra do Cipó National AND ALOUATTA CARAYA (PRIMATES: ATELIDAE) Park, Minas Gerais, Brazil. This new locality is at one of IN THE SERRA DO CIPÓ NATIONAL PARK, MINAS the highest elevations (1274 and 1254 m, respectively) yet GERAIS, BRAZIL recorded for these species (Carlos E. V. Grelle, pers. comm.; Maycon G. Belarmino, unpubl. data, respectively), at the Leonardo de Carvalho Oliveira westernmost limits of the Rio Doce basin, headwaters of Edeltrudes Maria V. C. Câmara the Rio Santo Antônio (Hirsch et al., 2002; see Fig. 1). André Hirsch, Ana Maria Oliveira Paschoal Rodrigo Martins Alvarenga, Maycon G. Belarmino Methods and Results
Introduction The study was carried out in a forest fragment with an ap- proximate area of 34.3 ha and a perimeter of approximately The Serra do Cipó National Park is 90 km north of Belo 3.22 km, in the municipality of Morro do Pilar, near the Horizonte, Minas Gerais, and part of the southern section neighboring municipality of Santana do Riacho (see Fig. 1). of the Serra do Espinhaço (19°12’ to 19°34’S, 43°27’ to Geographic coordinates and altitude were taken with a GPS 43°38’W). It is 33,800 ha in size, covering altitudes ranging device. We used a Landsat 5 TM satellite image (p218/r73, from 800 to 1600 m. The vegetation is a mix of cerrado (bush 01/nov/1997; Minas Gerais, DMC/IEF, 2001) to identify savanna), campo rupestre (rocky moorland), open pasture and the vegetation in the surrounding areas, and ArcGIS 8.2 gallery forests, with some forest patches on the eastern ridge. software (ESRI, 2001) for calculating the forest fragment’s Here we report unusual high-altitude sightings, made as part contour, area and perimeter. From the examination of the of an ongoing project, of two eastern Brazilian primate spe- satellite image done by Hirsch (2003), the study site may cies: Callithrix geoffroyi and Alouatta caraya. be characterized as a small semi-isolated fragment, linked on only one side with a gallery forest that follows a small Geoffroy’s marmoset, Callithrix geoffroyi (É. Geoffroy in watercourse downstream. The surroundings are occupied Humboldt, 1812), is endemic to the Atlantic forest of with rocky moorland and open pasture (Fig. 1). Brazil (Rylands et al., 1993; Fonseca et al., 1996). It is found in secondary forests in lowlands, semi-deciduous Two marmosets, Callithrix geoffroyi, were heard and seen in forests, gallery forest and forest borders, with a prefer- the forest fragment in August 2002. We later observed 10 ence for disturbed rather than mature areas (Passamani individuals there during a return visit in March 2003. The and Rylands, 2000a, 2000b). It is diurnal, and its diet is GPS coordinates taken in the field were 19°15’28”S and composed largely of fruits, exudates and small animal prey. 43°31’01”W, and the altitude was 1274 m. On 15 March Populations of Geoffroy’s marmoset are declining over large 2003, two members of the field team observed one individual parts of its relatively restricted range due to habitat loss and of Alouatta caraya in the same forest fragment, at approxi- fragmentation, hunting and capture for pets. Its distribution mately the same coordinates and at an altitude of 1254 m. appears to be further limited by its restriction, in many parts All the records were taken ad libitum (Altmann, 1974). of its range, to altitudes between sea level and 600-800 m (Mendes, 1997). Discussion
The black howler monkey, Alouatta caraya (Humboldt, Callithrix geoffroyi 1812) is typical of the Cerrado biome, but may also be Although little studied, the home range of C. geoffroyi found in forests along the Paraná/Paranaíba rivers, in de- is believed to vary from 20 to 30 ha (Rylands and Faria, ciduous forests in Caatinga regions of north-east Brazil, 1993). Passamani and Rylands (2000a, 2000b) estimated a semi-deciduous forests of the Pantanal, the humid Chaco of home range of 23.3 ha for a group of 3-5 individuals in a Argentina, and in “capões” – forest patches – of Rio Grande forest fragment of 110 ha in the state of Espírito Santo. The do Sul and extreme northwestern Uruguay (Hirsch et al., record from this study was made in a fragment of approxi- 2002). This species thus has a wide geographic range, from mately 34 ha, which suggests that its area is insufficient to northern Argentina to the northeast of Brazil. A. caraya is support more than one group. Considering a circle as the usually to be found in low altitudes up to approximately best shape, the ideal perimeter calculated with the formula 86 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 87
Figure 1. Location of the forest fragment where Callithrix geoffroyi and Alouatta caraya were recorded at the Serra do Cipó National Park, Minas Gerais, Brazil.
provided by Hirsch (2003) for this forest fragment is only altitudes (1254 m) recorded for the species (Maycon G. 2.08 km. The actual contour (3.22 km) is larger and some- Belarmino, pers. obs.), which extends its potential geo- what irregular, with a considerable edge effect acting on the graphical distribution and suggests that new proposals for interior forest area. population management might be implemented in areas previously considered unsuitable for the species. One of the causes of the threatened status of C. geoffroyi is its relatively restricted distribution in a highly fragmented Small and isolated fragments such as this one may not have environment. Our record of this species at an altitude of sufficient core area to support viable populations of many 1274 m extends its vertical range by almost 500 m, thereby species (Zudeima et al., 1996). They may function, how- indicating that it may be more wide-ranging than previ- ever, as an ultimate refuge for many species (Shafer, 1995). ously thought. This is also the westernmost record of the Small populations found in such small refuges may be sub- species in the Rio Doce basin (Hirsch et al., 2002). The ject to a series of stochastic processes of demographic, genetic nearest record on the western slopes of the Serra do Cipó and environmental origin that may lead them to extinction, National Park is of Callithrix penicillata, near the park’s despite measures taken for their conservation (Gilpin and administrative headquarters. Thus, the Serra do Cipó may Soulé, 1986; Brito and Fernandez, 2000). The negative ef- be considered a biogeographic divide between these two fects of population isolation, especially on small populations, marmoset species (Hirsch et al., 2002). have already been well-demonstrated in the conservation literature (see, for example, Meffe and Carol, 1997). Alouatta caraya Home range size for the genus Alouatta is reported to Although small forest fragments cannot support marmoset vary from 4.1 to 182 ha (Chiarello, 1993; Palacios and or howler populations which are viable in the long-term, Rodriguez, 2001). In fragmented landscapes, A. caraya has they may serve as “stepping stones” between larger forests, been registered in patches of 2 ha (Bicca-Marques, 1992; thereby facilitating gene flow and recolonization through Bicca-Marques and Calegaro-Marques, 1995). Their abil- dispersal and migration. These new records are in a large ity to incorporate secondary vegetation in their diet may protected area, the Serra do Cipó National Park, surround- explain their capacity to survive in small and degraded areas ed by the buffer zone of the Morro da Pedreira Environ- (Chiarello, 1994). This observation is one of the highest mental Protection Area. This allows for some hope for the 88 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 89 long-term persistence of these populations. Future research ESRI. 2001. ArcView GIS v. 8.2. Environmental Systems may reveal the conservation relevance of such small frag- Research Institute, Redlands, CA. Website:
Shaffer, C. L. 1995. Values and shortcomings of small re- serves. BioScience 45: 80-88. Zudeima, P. A., Sayer, J. A. and Dijkman, W. 1996. Forest fragmentation and biodiversity: The case for intermediate- sized conservation areas. Environ. Conserv. 23: 290-297.
DISTRIBUIÇÃO DO GUIGÓ (CALLICEBUS COIMBRAI) NO ESTADO DE SERGIPE
Marcelo Cardoso de Sousa
Sergipe é o menor estado brasileiro em extensão territorial. Possui cerca de 21.994 km² e localiza-se na região nordeste do Brasil, ao sul do Rio São Francisco. Seu relevo apresenta formas desgastadas, com altitudes pouco elevadas; cerca de 86% do território é abaixo de 300 m sobre o nível do mar. A baixada litorânea constitui uma extensa faixa de tabuleiros sedimentares, com cerca de 150 km de largura do litoral, em direção ao interior, cortada pelas várzeas dos rios (Vaza-Barris, Sergipe, Piauí, Real) que deságuam no Oceano Atlântico. No norte do estado, esses terrenos baixos se unem à planície aluvial do Rio São Francisco, o maior rio de Sergipe, o qual demarca a divisa com o estado de Alagoas. A baixada, por seus aspectos fisiográficos, corresponde em sua maior parte à Zona da Mata, cuja Figure 1. Ocorrência do guigó Callicebus coimbrai no estado vegetação original era a floresta tropical, hoje em grande do Sergipe, Brasil. Escala 1:3.000.000. Projeção Área Igual parte devastada pela exploração econômica predatória ou Cilíndrica. Mapa gentilmente confeccionado por Mark Denil, substituída por áreas agrícolas. GIS and Mapping Laboratory, Center for Applied Biodiversity Science, Conservation International, Washington, DC. Em meio às áreas antrópicas, ainda existem remanescentes florestais, pequenas ilhas de vegetação secundária 1. Mata da Santana (10°32’S, 36°44’W). Localizada entre representadas por formações do tipo Floresta Ombrófila os municípios de Pacatuba e Japoatã, nos arredores da Densa e Floresta Estacional Semidecidual. Vários desses localidade tipo de Callicebus coimbrai, a mata da Santana remanescentes florestais foram percorridos nos últimos é um fragmento com cerca de 150 ha, isolada em meio anos com o propósito de se registrar a presença de Calli- a plantações de cana-de-açúcar. A maior parte da mata cebus coimbrai e ampliar o conhecimento sobre as suas áreas é constituída por vegetação secundária, entretanto, al- de ocorrência. Apesar de incluída na nova lista da fauna gumas árvores altas remanescentes com cerca de 20 m brasileira ameaçada de extinção, C. coimbrai dispõe de de altura ainda podem ser encontradas, principalmente, pouquíssimos registros de campo, e sua distribuição e estado nas grotas e encostas de difícil acesso. A retirada seletiva de conservação ainda não estão efetivamente bem definidos. de madeira é uma das principais ameaças à integridade As únicas informações sobre essa espécie foram fornecidas da mata e à sobrevivência dos Callicebus. Outro fator de por Kobayashi e Langguth (1999) quando, no trabalho da risco é a possibilidade de incêndios na floresta, uma vez descrição da espécie, indicaram duas áreas de ocorrência de que durante a colheita da cana-de-açúcar todo o canavial, C. coimbrai, além da sua localidade tipo no estado de Sergipe. inclusive próximo à borda da floresta, é incendiado para Sousa (2000) acrescentou mais três localidades, uma delas facilitar o manejo da safra. Observamos, ouvimos e obtive- situada no nordeste do estado da Bahia. Van Roosmalen et al. mos gravações de três indivíduos de C. coimbrai no dia 4 (2002) fizeram uma compilação das informações até então de julho de 2003. disponíveis e sugeriram os limites de sua distribuição entre o Rio Itapicuru (ao norte) e o Rio São Francisco. 2. Mata do Serigy (10°33’S, 36°42’W). No município de Pacatuba, próxima à mata da Santana, com aproximadamente Neste nota, reportamos novos registros da distribuição de 70 ha de área, a mata do Serigy encontra-se hoje bastante Callicebus coimbrai baseados em observações realizadas alterada. Destaca-se na área uma vegetação secundária, no período de outubro de 2002 a setembro de 2003, muitas clareiras em processo de sucessão ecológica e muitas durante nossos trabalhos de campo desenvolvidos no espécies heliófitas, inclusive gramíneas e ciperáceas que estado de Sergipe. Nesse período, tivemos a oportunidade dificultam o acesso ao seu interior. A fisionomia atual da de registrar a vocalização de Callicebus em 14 fragmentos mata do Serigy é conseqüência de um incêndio ocorrido florestais e obter imagens de alguns indivíduos em há aproximadamente oito anos que destruiu boa parte duas localidades. da mata. Apesar do seu estado de perturbação, Callicebus 90 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 91 coimbrai ainda pode ser encontrado no local. Registramos 9. Mata do Junco (10°32’S, 37°03’W). Às margens de sua vocalização no dia 28 de setembro de 2002. uma pequena estrada e cercada por pequenos povoados do município de Capela, a mata do Junco possui cerca de 400 3. Mata do Oiteiro (10°39’S, 37°03’W). Situada no ha. Mescla trechos de mata devastada, encraves de cerrado e município de Rosário do Catete, em meio a uma vegetação áreas relativamente conservadas, principalmente nos baixios de cerrado, a mata do Oiteiro localiza-se num pequeno e ao longo de pequenos riachos. Registramos a vocalização vale onde a vegetação possui um maior porte. O estrato de Callicebus coimbrai no dia 14 de junho de 2003. arbóreo da mata possui entre 10 a 15 m, contudo, algumas árvores emergentes podem ultrapassar os 20 m. O interior 10. Mata da Nova Descoberta (11°06’S, 37°19’W). da mata encontra-se parcialmente devastado, sendo a caça Ouvimos a vocalização de Callicebus coimbrai no dia 29 de e a retirada de madeira constantes; contudo, pudemos março de 2003, num trecho de mata parcialmente devastada ouvir a vocalização de C. coimbrai no dia 20 de junho do município de Itaporanga d’Ajuda. A mata localiza-se às de 2003. margens da rodovia estadual SE-270, ao lado do povoado Nova Descoberta. As pressões sofridas pela mata são 4. Mata do Cadoz (10°23’S, 36°39’W). Em meio a geradas pela expansão desse pequeno núcleo urbano cujos pastagens, plantações de coqueiros, algumas lagoas e de habitantes utilizam a madeira, caçam e desmatam para uma fazenda de criação de peixes e gado, no município expandir suas lavouras. de Neópolis, encontra-se a mata da Fazenda Cadoz. A mata, uma capoeira alta, encontra-se relativamente bem 11. Mata da Fazenda Trapsa (11°12’S, 37°14’W). No conservada e em estágio de recuperação. O registro da município de Itaporanga, numa área de Cerrado bastante vocalização de Callicebus coimbrai foi feito no dia 30 de deteriorado (devido a construção de uma represa e a julho de 2003. exploração de uma jazida de cascalho laterítico) situado no antigo terraço marinho de formação geológica do grupo 5. Mata da Serra Preta (10°30’S, 37°37’W). Reduzida às barreiras, alguns trechos de mata encontram-se nos vales e encostas de uma elevação de pouca altitude, denominada nos terrenos baixos. Nesses locais, a vegetação apresenta-se Serra Preta, no município de Frei Paulo. A mata encontra- mais densa, e possui um estrato arbóreo entre 5 e 15 m, se seriamente ameaçada pela expansão de pequenas lavouras cujas árvores apresentam geralmente um pequeno diâmetro. de subsistência que avançam no sentido do sopé até o alto A exploração de madeira já foi intensa no local, e a presença do morro. Fizemos o registro da presença de Callicebus de árvores mortas com cerca de 20 m evidenciam incêndios coimbrai no dia 5 de julho de 2002. ocorridos num passado não muito distante. A mata hoje encontra-se em recuperação, embora a extração de madeira 6. Mata da Fazenda Sabão (11°30’S, 37°34’W). Uma das continue. A caça, embora proibida pelo proprietário da principais características dos remanescentes florestais da fazenda, persiste no local. Registramos a vocalização de Fazenda Sabão, situada no município de Indiaroba, é a Callicebus coimbrai no dia 28 de abril de 2002. grande quantidade de palmeiras do gênero Attalea em meio a uma formação arbórea densa e, em maiores proporções, 12. Mata do Crasto (11°22’S, 37°25’W). Localizada no áreas de capoeira alta. Na mata, que possui aproximadamente município de Santa Luzia do Itanhy, possui uma área 300 ha, obtivemos registros da vocalização de Callicebus de aproximadamente 900 ha. É um dos remanescentes coimbrai no dia 2 de maio de 2003. florestais mais significativos e conservados do estado. Só subsiste graças à proteção dos proprietários que vêm 7. Mata da Aiumas (10°25’S, 36°39’W). A Fazenda Aiumas tentando garantir a integridade da floresta. A mata do localiza-se as margens da rodovia estadual SE-204, no Crasto foi decretada Reserva Particular de Patrimônio município de Pacatuba. A área florestada da Fazenda Natural (RPPN) no dia 10 de agosto de 1989 pela Portaria encontra-se bastante perturbada, reflexo da retirada de No. 442/89 do Instituto Brasileiro do Meio Ambiente e madeira para lenha e estacas para cercas. Contudo, existe dos Recursos Naturais Renováveis (IBAMA). As principais na área um pequeno trecho de mata ciliar, entremeada com ameaças à mata do Crasto são os projetos de expansão palmeiras dos gêneros Attalea e Elaeis, em bom estado de turística propostos a partir da pavimentação asfáltica de conservação. Fizemos o registro de Callicebus coimbrai no estradas de terra já existentes no entorno e até mesmo dia 30 de julho de 2003. dentro de alguns pontos da mata, além da retirada de madeira e da caça que ainda ocorrem clandestinamente e 8. Mata da Aguada (10°40’S, 36°56’W). Possui cerca de de forma sistemática na área. No dia 4 de maio de 2003 40 ha e está situada no município de Carmópolis, nos ouvimos a vocalização de Callicebus coimbrai e conseguimos arredores do Povoado Aguada. Registramos a presença de visualizar um indivíduo cruzando por sobre as árvores uma Callicebus coimbrai nesse fragmento florestal, relativamente das trilhas existentes no interior da mata. conservado e situado na encosta e no alto de um pequeno morro, no dia 31 de julho de 2003. Segundo informações 13. Mata do Dira (10°53’S, 37°21’W). Os remanescentes colhidas através de depoimentos de moradores do local, florestais da Fazenda Dira somam hoje pouco mais de 100 a retirada de madeira não é permitida, embora ocorra às ha. A mata depauperada ainda existente está sob a proteção escondidas, mas, a caça ainda persiste no local. dos proprietários e é um testemunho do que foi um dos 90 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 91
mais importantes remanescentes de Mata Atlântica daquela Sousa, M. C. 2000. New localities for Coimbra-Filho’s titi região do estado, destruída pela expansão de pastagens para monkey, Callicebus coimbrai, in North-east Brazil. Neo- a criação de gado, pela caça e pelos assentamentos para a trop. Primates 8(4): 151. reforma agrária. Registramos a vocalização de Callicebus Van Roosmalen, M. G. M., Van Roosmalen, T. e coimbrai no dia 23 de agosto de 2003. Mittermeier, R. A. 2002. A taxonomic review of the titi monkeys, genus Callicebus Thomas, 1903, with the 14. Mata da Arauari (10°45’S, 36°59’W). Localizada no description of two new species, Callicebus bernhardi município de Santo Amaro, a mata da Arauari foi visitada and Callicebus stephennashi, from Brazilian Amazonia. por Langguth e Kobayashi em 1995 quando, na ocasião, Neotrop. Primates 10(Suppl.): 1-52. eles coletaram uma série de dois parátipos para a descrição da espécie. No dia 14 de maio de 2003, percorremos um trecho da mata na qual ouvimos e observamos dois ESTIMATIVA DE DENSIDADE E TAMANHO indivíduos. Constatamos a retirada recente de madeira da POPULACIONAL DE SAUÁ (CALLICEBUS NIGRIFRONS) área e a destruição das bordas da floresta para a formação de EM UM FRAGMENTO DE MATA EM REGENERAÇÃO, pastos e de pequenas lavouras. VIÇOSA, MINAS GERAIS, BRASIL
Com base nas observações realizadas em vários fragmentos Regiane C. Romanini de Oliveira florestais do estado, principalmente naqueles nos quais Andressa Sales Coelho conseguimos registrar a presença de Callicebus coimbrai, Fabiano R. de Melo podemos argumentar o seguinte: Introdução a. Todas as áreas florestadas do estado de Sergipe encontram-se sob forte processo de degradação, inclusive Primatas são importantes indicadores para as florestas aquelas que são redutos das diminutas populações de tropicais como componente fundamental de estratégias C. coimbrai. para a conservação da biodiversidade, tanto em nível regional quanto de bioma (Rylands et al., 1997). A b. Apesar de persistirem em alguns fragmentos e terem su- Floresta Atlântica, que retém atualmente 7,5% de sua portado ao longo dos anos a deterioração de seus ambientes, vegetação primária (Myers et al., 2000), abriga 23 espécies as populações de C. coimbrai acham-se em franco declínio, e subespécies reconhecidas de primatas, onde 74% delas principalmente devido à caça, redução e conseqüente perda são endêmicas. Esta região também apresenta o segundo de habitat. maior número de taxa ameaçados, 18, sendo endêmicos e compreendendo 78% dos primatas ocorrentes na Floresta c. A soma de todos os fragmentos onde a espécie ainda ocorre Atlântica (Rylands et al., 1997). totaliza pouco mais de 5000 ha distribuídos em pequenas áreas, nenhuma delas legalmente protegida (a exceção da O sauá, Callicebus nigrifrons, ocorre na região sudeste RPPN Mata do Crasto). Essa falta de proteção e fragilidade (Kinzey, 1982). Encontra-se listada como “vulnerável” no do ponto de vista de conservação, além do tamanho reduzido estado de Minas Gerais (Machado et al., 1998) mas infor- de sua área de distribuição até o momento conhecida, faz de mações a cerca da sua biologia e ecologia permanecem ainda C. coimbrai uma das espécies de primatas mais ameaçadas do escassos. Dados de densidade podem ser de grande utili- mundo. A ampliação do conhecimento sobre essa espécie, dade para o estudo das conseqüências da fragmentação do a busca de novas áreas de ocorrência, a criação de áreas habitat, como por exemplo para avaliar o “status” de uma protegidas e o estabelecimento de programas de proteção população que se encontra ameaçada (Laurance, 1990). são medidas que se fazem urgentes e imprescindíveis para a Este trabalho teve como objetivo fornecer uma estimativa garantir a sobrevivência da espécie. da densidade e do tamanho populacional de Callicebus ni- grifrons sobreviventes em um pequeno fragmento de mata Agradecimento: À Fundação O Boticário de Proteção à em processo de regeneração. Natureza pelo suporte financeiro parcial para a realização do estudo. Área de Estudo e Métodos
Marcelo Cardoso de Sousa, Laboratório de Zoologia, Os censos foram conduzidos numa área de aproximadamente Instituto de Tecnologia e Pesquisa, Universidade Tiradentes, 75 ha no município de Viçosa, Minas Gerais, Brasil Avenida Murilo Dantas 300, Aracaju 49032-490, Sergipe, (20°45’S e 42°51’W), em terreno de relevo montanhoso e Brasil. E-mail:
A coleta dos dados foi feita usando o método dos transectos m, indicando uma certa preferência da espécie por estratos lineares (Buckland et al., 1993), no período de fevereiro a superiores da mata. Foi registrado uma taxa de encontros junho de 2000, a partir de quatro trilhas (Trilha 1 = 930 de 1,83 grupos/10 km de censo, enquanto Chiarello e Melo m, 4 = 950 m, A = 520 m e D = 400 m) feitas de maneira (2001) obtiveram, para diferentes fragmentos florestais no a cobrir os diferentes tipos florestais do fragmento. Um Espírito Santo, uma variação de 0,22 a 1,66 grupos/10 km total de 60,24 km de trilhas foi percorrida (comprimento de censo. Pinto et al. (1993) registraram um valor de 0,54 total do transecto) durante 76:56 horas de observação. As grupos/10 km de censo para a Reserva Biológica Augusto 94 amostras de censo realizadas nesse período foram feitas Ruschi (Tabela 1). predominantemente pela manhã (63%) entre 08:00 h e 12:00 h, horário de maior atividade dos primatas. Esforços A partir das distâncias perpendiculares, o programa foram feitos para manter a velocidade de caminhada sempre Distance determinou a ESW ou largura efetiva da trilha, constante e próxima de 1,5 km/h. A análise dos dados se que foi de 18,98 m, e uma densidade de 14,86 indivíduos/ deu através do programa Distance versão 2.1 (Laake et km². Esta se encontra dentro da variação registrada para al., 1994), que se baseia nas distâncias perpendiculares outras regiões de Mata Atlântica (Chiarello e Melo, registradas durante o censo. As densidades foram calculadas 2001; Pinto et al., 1993) e se mostra relativamente alta, em grupos/km², fazendo a multiplicação da densidade de indicando uma elevada densidade de sauás no fragmento, grupo pelo seu tamanho médio. se comparado às densidades de fragmentos maiores (Tabela 1). Podemos inferir que pela falta de grandes predadores, Resultados e Discussão os fragmentos pequenos suportam uma densidade maior de sauás que os fragmentos maiores. Um outro fator de Um total de 11 encontros visuais foram registrados durante extrema importância que pode afetar o sucesso de espécies o estudo. O tamanho médio dos grupos foi de 3,09 frugívoras, como o sauá, é a falta de recursos, especialmente indivíduos. Em trabalho realizado com C. personatus por frutos. A sobrevivência desses animais num fragmento Pinto et al. (1993) na Reserva Biológica Augusto Ruschi, pequeno como a Mata da Biologia é provavelmente o tamanho médio dos grupos foi de 3,9 indivíduos, devida, em parte, à ocorrência de várias espécies de árvores enquanto que 6 indivíduos/grupo foram encontrados que oferecem frutos carnudos e também à forma como se na Reserva Biológica de Sooretama por Kinzey e Becker encontram distribuídas. Como sabemos, em fragmentos (1983). A altura média de detecção dos grupos foi de 18 pequenos as árvores frutíferas se distribuem melhor no
Figura 1. A localização da Mata da Biologia, um fragmento de floresta de 75 ha no campus da Universidade Federal de Viçosa, Viçosa, Minas Gerais. 92 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 93
Tabela 1. Densidades estimadas para as espécies de Callicebus registradas para as várias localidades de floresta Atlântica. Densidade Taxa de avistamento Espécie Localidade/Estado Área (km²) Fonte (indiv./km²) (grupos/10 km) C. personatus M7/317, Espírito Santo 1,4 0,22 2,6 1 C. personatus Reserva Biológica Augusto Ruschi, Espírito Santo 5,4 0,54 40,0 2 C. personatus Putiri, Espírito Santo 6,4 1,02 2,1 1 C. personatus Reserva Florestal Linhares (CVRD), Espírito Santo 7,7 1,23 218,0 1 C. nigrifrons Fazenda Barreiro Rico, São Paulo 7-10 - 32,6 2 C. personatus Reserva Biológica de Sooretama, Espírito Santo 9,5 1,66 242,5 1 C. melanochir Una, Bahia 3,4-16,7 - 1,0 2 C. nigrifrons Serra do Brigadeiro, Minas Gerais 10,3 - 132,1 3 C. melanochir Estação Experimental Lemos Maia (CEPLAC), Bahia 17,0 - 10,0 4 C. melanochir Fazenda Teimoso, Bahia 17,7 - 2,4 2 C. nigrifrons Viçosa, Minas Gerais 14,86 1,83 0,75 Neste estudo Fonte: 1: Chiarello e Melo (2001); 2: Pinto et al. (1993, compilado); 3: Cosenza e Melo (1998); 4: Müller (1996).
espaço e no tempo, levando espécies frugívoras a ampliar a Ciências Ambientais, Centro de Biociências e Tecnologia, sua área de uso (Milton e May, 1976). Universidade do Norte Fluminense, Rio de Janeiro, Brasil, e-mail
Machado, A. B. M., Fonseca, G. A. B. da, Machado, R. B., baka, also referred to as the Brokopondo Reservoir of the Aguiar, L. M. S. e Lins, L. V. 1998. Livro Vermelho das Suriname River, and the northern edge of the park is ap- Espécies Ameaçadas de Extinção da Fauna de Minas Gerais. proximately 3.0 km from the village of Brownsweg. Fundação Biodiversitas, Belo Horizonte. Melo, F. R. e Mendes, S. L. 2000. Emissão de gritos longos The origin of the village and the lake corresponds to the por grupos de Callicebus nigrifrons e suas reações a playbacks. damming of the Suriname River in 1964 for construction Em: A Primatologia no Brasil – 7, C. Alonso e A. Langguth of one of the first hydroelectric plants in South America. (eds.), pp. 215-222. Sociedade Brasileira de Primatologia e Half the territory of the Saramaccan people was flooded as a Editoria Universitária, João Pessoa, Paraíba. result of the construction of the dam. Approximately 4,500 Milton, K. e May, M. 1976. Body weight, diet and home people from three autonomous villages were relocated to range area in primates. Nature, Lond. 259: 459-462. Brownsweg, although De Dijn now estimates the popula- Müller, K. H. 1996. Emigration of a masked titi monkey tion to be about 3,500 residents. The Brownsberg is valu- (Callicebus personatus) from an established group, and the able for its floristic and faunal diversity (as yet undiscovered foundation of a new group. Neotrop. Primates 4(1): 19-21. for most taxonomic groups), and also for the educational Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, opportunity it provides to the citizens of Suriname, most G. A. B. da e Kent, J. 2000. Biodiversity hotspots for especially in the highly populous Brownsweg. conservation priorities. Nature, Lond. 403: 853-858. Pinto, L. P. S., Costa, C. M. R., Strier, K. B. e Fonseca, G. A. The Brownsberg has long been a destination for tourists, B. da. 1993. Habitat, density and group size of primates in particularly from Holland, but the proximity of the park to a Brazilian tropical forest. Folia Primatol. 61: 135-143. Paramaribo also attracts day-trippers and over-night tour- Rylands, A. B., Mittermeier, R. A. e Rodriguez-Luna, E. ism from Surinamers. This has resulted in a recent increase 1997. Conservation of Neotropical primates: Threatened in the number of dwellings in the park to accommodate a species and an analysis of primate diversity by country few dozen permanent staff, tourists, and researchers on the and region. Folia Primatol. 68: 134-160. top of the berg, besides considerable forest clearing on the Valverde, O. 1958. Estudo regional da Zona da Mata de eastern slope of the plateau for picturesque “outlooks” over Minas Gerais. Rev. Brasil. Geog. 1: 3-38. the forest and lake below. The berg itself rises 473 m above the relatively flat surrounding terrain (50 m above sea level) (Reichart, 1997). The flora is extremely diverse, supporting PRIMATES OF BROWNSBERG NATUURPARK, not only low-elevation species, but also a flora indicative SURINAME, WITH PARTICULAR ATTENTION TO THE of cloud forest on the top of the berg and intermediate PITHECIINS climatic conditions on the slopes. Huber (1995) character- ized Guayana Shield elevations of 500 m or more as cool Marilyn A. Norconk, Mary Ann Raghanti and wet (submesothermic [mean annual temperature 18- Sara K. Martin, Brian W. Grafton 24 °C], ombrophilous [rainfall >2000 mm]), with fewer L. Tremaine Gregory, Bart P. E. De Dijn than two dry months a year. An informal census by P.-M. Forget (pers. comm.), consisting of a single transect from Introduction the lake in the east, up to and across the plateau and down the northern side of the berg, suggested that the Browns- Brownsberg Natuurpark (5°01’N, 55°34’W) is Suriname’s berg is more floristically diverse in flowering plant species only wildlife park that is open and accessible to both Suri- than either Nouragues in French Guiana (see Bongers et name citizens and researchers. The park lies 130 km south al., 2001) or the Central Suriname Nature Reserve (pre- of the capital, Paramaribo, and consists of a lateritic plateau, viously Raleighvallen-Voltzberg). All three sites are on which at 530 m forms the top of the Brownsberg range. the Guiana Shield, where 6.6% of plant genera and 40% The plateau lies 473 m above the surrounding lowlands and of plant species are endemic (Berry et al., 1995, p.165). is relatively humid with low cloud cover, particularly on the Fitzgerald (2003) conducted a year-long wildlife survey on eastern perimeter. The Brownsberg range has at least one the Brownsberg from November 2000 to May 2002. Her additional lateritic plateau at some 100-150 m above sea census included primates, though not as a focus, but the level, which is much drier than the upper one. In between work she initiated has been incorporated into a long-term the two plateaus are slopes with exceptionally high forest, monitoring program projected to extend until 2006. but also occasional broad ridges or narrow semi-plateau areas with lateritic soil (e.g., at 200-350 m elevation) and The plateau and surrounding area of the Brownsberg have medium to low forest. The areas with thick laterite crusts long been known to miners for their gold and bauxite (perhaps 10% of the park), especially where the forest is reserves. In 1908, weekly trains transported gold from low, are dominated by the Myrtaceae in all storeys (B. P. the Brownsberg area to Paramaribo, and gold has been E. De Dijn, unpubl. data). Forests range from seasonally mined in the area since 1718 (Reichart, 1997). In 1916, dry to seasonally flooded, consisting of both secondary and the Surinam Bauxite Company (SURALCO, a subsidiary primary forest, steep forested slopes, and creek-side forest of ALCOA-US) purchased the mountain and continues to in the valleys – a total area of c. 8,000 ha (Reichart, 1997). hold mineral rights to the Brownsberg. Suriname’s Foun- The eastern edge of the plateau is bounded by Lake Afo- dation for Nature Conservation (STINASU) received a 94 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 95
75-year lease to the plateau and middle portion of the sess the mineral content of the berg. We estimated that mountain in 1970. In 2001, the park was expanded to 4.8 ha of forest along the main plateau road was destroyed 12,200 ha from its original 8,400 ha by the addition of by SURALCO for the construction of test pits in May pristine high forest in the southern portion of the Browns- 2003. Both forms of mining put the forests and their wild- berg range. At the same time, 1,000 ha in the northwest- life at risk, and the bauxite mining and reclamation of the ern part of the park was relinquished to local inhabitants plateau threatens the very existence of the park as an eco- (Fitzgerald et al., 2002). tourism resource uniquely accessible to all Surinamers.
Currently, gold mining provides a much-diminished return The purpose of this census was to gather data specific to pri- compared to the value-to-effort return of the early 20th mate populations, conduct a feasibility study to prepare for century, but mining practices involving heavy equipment, a long-term study of pitheciin primates, and to contribute water-powered extraction and the perfusion of stream to the database being created by STINASU to ensure long- beds with mercury are causing more damage than previ- term protection of the site. ous methods. Fitzgerald et al. (2002, p.2) characterized Brownsweg as “a large village with a busy small-scale gold Methods mining industry.” Our recent observations suggest that the level of production and speed of processing has destroyed The census was conducted for 28 consecutive days, from hundreds of meters of pristine streambeds draining the 21 May to 17 June 2003, during the early rainy season. Brownsberg since March 2003. Gold mining is also more Two research teams, of two to three people each, censused actively pursued today than bauxite mining, but the threat all trails and roads on the plateau of the Brownsberg every of destruction on the plateau itself is not without devastat- other day (Table 1). The censused area included slopes ing consequences. SURALCO has recently brought crews leading east to Lake Afobaka and north toward the village with survey equipment to the plateau in order to reas- of Brownsweg. We began transect walks at 06:15 hrs and
Figure 1. The Mazaroni plateau, encompassed within the 450 m topographical line, of Brownsberg Natuurpark, Suriname. Positions of the main road (dark line) and approximate position of trails (dotted lines) both on the plateau and descending the slopes of the mountain are indicated. 96 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 97
Table 1. Characteristics and length of trails that were used as transects for the census, and the total distance walked on each trail. The length of transect was not the entire length of the trail for AKP, Witi Kreek, and Jeep Trail. The elevation change is taken from the top of the plateau at 473 m. Elevation changes are estimates. Trail Name Trail characteristics Length of trail (km) Total distance walked (km) Elevation change from the plateau1 AKP Plateau & slope 3.6 62.2 - 250 m Jeep Trail Plateau & slope 3.1 58.6 - 300 m Mazaroni Val Plateau & slope 1.0 16.9 - 150 m Irene Val Plateau & slope 2.0 10.3 - 300 m Kumbu Val Plateau & slope 1.5 6.0 - 150 m Witi Kreek Slope & creek side 3.5 63.4 - 450 m Mazaroni Weg Plateau 3.0 70.7 0 Rondwandeling Plateau 2.3 37.4 0 Tele Sur Plateau 1.3 21.9 0 Mazaroni Top Plateau 0.7 8.4 + 10 m (1From Appendix C: Fitzgerald et al., 2002.) ended at approximately 14:30 hrs. Walking speed was ap- 10 km using body weight data from Ford and Davis (1992) proximately 1.3 km/hr. We collected the following data multiplied by individual ER. each time a primate group or individual was detected: time of day and weather, location (trail mark), observation of pri- We also compared primate sightings on plateau vs. slope mate species (height, distance, and direction from the trail), trails to assess variations in local abundance using non- group size and age/sex composition data, and activity at the parametric statistics (-values were set at 0.05). Relative time of the sighting. Species encountered informally, i.e., trail abundance is reported as the number of times a species not part of transect walks, were not treated in the analysis. was encountered divided by the number of times the trail was walked. Species abundance was calculated as the relative Data were recorded in both directions of our travel route frequency of encountering a particular species on any trail. (“transect” and “return transect”) since all but one of the trails (Rondwandeling) were linear. Visibility on either side Results of the trail varied, ranging from approximately 5 m to 25 m. We discarded any data that could have represented repeated All eight primate species found in Suriname were seen at sampling of a species or group and, for the analysis below, the Brownsberg. Alouatta seniculus was very abundant at also eliminated all data collected on primate vocalizations. the site, with an estimated 20 groups encountered, the None of the primates were habituated to observers, but highest biomass (PBER), and the second highest individual there were several cases in which we were able to accumu- encounter rate (ER) (Table 2). Howlers were encountered late sufficient data to calculate group size and composition on all trails save one, but were seen on that trail during with confidence. Nevertheless, the summary statistics that informal observations. Group sizes were relatively small, we report are considered to be minimum estimates. ranging from 2 to 7 individuals, but the groups were well distributed both on the plateau and slopes of the Browns- Positional data on trail locations were collected prior to the berg (Table 3). onset of our study by K. Fitzgerald, S. Mitro, and B. P. E. De Dijn, using a Garmin GPS 12 XL. Satellite readings were Chiropotes satanas had the highest estimated individual taken every 100 m. We measured the road to Brownsweg ER due to their large group sizes (average = 32.7 indi- (AKP) that was also used as a census transect using a Garmin viduals, n = 3 groups) and relatively frequent encounters. eTrex Venture, again taking readings every 100 m. GPS data We observed three groups that were encountered mainly were entered into ArcView 3.2. Maps do not reflect eleva- on trails that transected the forested slopes of the berg, tional differences. although they were also seen on the plateau during infor- mal observations. They had the second highest PBER (see Individual encounter rates (ER) for each species (except Table 2). Saimiri and Ateles, for which data were insufficient) were calculated by dividing the total number of individuals The tamarins (Saguinus midas) had the third highest en- encountered by 26.2 km (total survey distance). Group counter rates. We estimated that we encountered 16 groups encounter rates were calculated in the same manner, and of S. midas with an average group size of 5.7 individuals (see both individual and group ER were expressed as groups en- Table 2). Like the howlers, the tamarins were common and countered per 10 km. We censused a total linear distance of seen on almost all trails during the survey. 364.2 km (see Table 1), an average of 12.26 ± 1.27 km/day. Thus each trail was censused approximately every two days. White-faced sakis (Pithecia pithecia) were relatively We estimated Primate Biomass Encounter Rate (PBER) per common, having the third highest group ER (n = 10). 96 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 97
Estimated group sizes ranged from 2 to 6 individuals (av- encountered C. apella most often on the plateau (Table 3), erage = 3.7 individuals), although small groups with 2 to but suspected that they too are wide-ranging in an area that 3 individuals may very well have been underestimated in includes at least the eastern slope of the berg. our counts. No groups were fully habituated and some were very skittish. Nevertheless, of those seen repeatedly, only Ateles paniscus were more often heard than seen. Subgroup one had more than one adult male (easily recognized by the size ranged from 2 to 4 (see Table 2). When encountered, males’ white faces). they first displayed by breaking off branches and hurling them down on observers, and then fled. We have little Cebus olivaceus were encountered quite frequently, but confidence in our population measures for Ateles. A single group sizes were difficult to estimate. An average group squirrel monkey group (Saimiri sciureus) was seen once; size of 12 is an underestimate, since a group of > 32 was their preference for stream-side terrain at the base of the encountered during informal (non-census) observations. berg may make them rare, or at least only seasonal visitors, C. olivaceus individuals were well-dispersed when encoun- on the plateau. tered (unlike Chiropotes that were also found in large, but more cohesive groups) and accurate group counts were We compared the trails that ran exclusively on the plateau not possible. Nevertheless, capuchins appeared to be rare with those that began on the plateau and then descended and very wide-ranging at the Brownsberg. We were more along the slopes of the berg (see Table 3). We found a non- confident with the count of a single group of Cebus apella significant trend for higher encounter rates on the slopes as which was seen on multiple occasions, both while collect- opposed to the flat plateau on the top of the berg (Wilcoxon ing transect data and during informal observations. We signed ranks test Z = 1.83, p = 0.07).
Table 2. Group size (minimum and range of group sizes) and number of groups observed during the census. Individual and group encounter rates (ER) were calculated from the group size data (see Methods). Primate biomass encounter rate (PBER) was calculated by multiplying body mass data (taken from Ford and Davis, 1992) by total number of individuals encountered / 10 km linear distance censused (after Wallace et al., 2000). Average observed Observed no. of Individual Group PBER Species group size (range) groups ER/10 km ER/10 km kg/10 km Saguinus midas 5.69 (3-8) 16 34.73 6.1 1.85 Pithecia pithecia 3.70 (2-6) 10 14.12 6.1 2.29 Saimiri sciureus – – – – – Cebus apella 14 1 5.30 0.4 1.45 Cebus olivaceus 12.0 (9-14) 3 13.70 1.1 3.68 Chiropotes satanas 32.67 (22-44) 3 37.40 1.1 10.66 Alouatta seniculus 4.65 (2-7) 20 35.50 7.6 22.72 Ateles paniscus* 2 (2-4) – – – – Total PBER 42.65 – Insufficient data, * Subgroup size.
Table 3. Relative primate encounter rate (ER) per trail, which equals the total number of primate encounters per trail per number of census walks (n). The column totals are the total number of sightings per species. With the exception of Rondwandeling, all the trails were linear and n represents the number of round-trips. Shaded rows are trails that traversed both plateau and slope; unshaded rows are trails that are found only on the plateau. Total encounters are the sum of plateau and slope and plateau only. Relative Trail (n walks) S. midas S. sciureus P. pithecia C. apella C. olivaceus C. satanas A. seniculus A. paniscus ER/trail AKP (10) 7 2 2 5 5 4 0.417 Jeep (9) 3 3 1 2 3 5 0.315 Mazaroni Val (9) 1 3 1 0.185 Irene Val (4) 2 1 1 0.333 Kumbu Val (4) 1 1 1 0.250 Witi Kreek (9) 5 1 5 2 1 5 3 0.349 Mazaroni Weg (17) 10 4 1 3 1 0.224 Rondwandeling (18) 9 10 4 1 9 0.367 Tele Sur (9) 1 1 3 2 0.194 Mazaroni Top (7) 1 1 1 0.143 Total enounters/spp. 18/20 1/0 11/16 1/6 7/2 13/3 18/14 7/1 98 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 99
Discussion
Average group size for A. seniculus at the Brownsberg was small compared with a number of group size estimates from other seniculus populations (range 4.25 to 10.5). However, our estimated group size was similar to that found by Mit- termeier (1977) at the Central Suriname Nature Reserve (where there was no hunting), and also similar to the sizes observed by Bennett et al. (2001) on the Río Tapiche in Peru (where hunting was reported as severe). We have no evidence that Alouatta is being hunted within the area that was censused at the Brownsberg, although there are reports of hunting primates inside the reserve near the margin of Lake Afobaka. If the larger group size reported from the llanos of Venezuela is excluded, there is relatively little Figure 2. Comparison of group size estimates for the eight species variation in red howler group sizes (mean 5.23 ± 0.21, n = of primates found at the Brownsberg. Data are from: Defler 6 studies) (Fig. 2). (1982, 2003), Janson (1985 in Sussman, 2000), Kessler (1998), Mittermeier (1977), Muckenhirn (1975), Simmen et al. (2001), With regard to pitheciins, we documented the largest re- Terborgh (1983), and this census. ported groups of Chiropotes satanas, ranging from 22 to 44 individuals, larger than maximum estimates by Mittermeier (1977: 27 individuals) in Suriname or Muckenhirn et al. Low species encounter rates for Saimiri sciureus may also (1975: 20 individuals) in Guyana. Lehman et al. (2001) have been an artifact of the season, but the habitats pre- recently examined variation in group size and number of ferred by Saimiri only occurred on one trail, the streamside adult males and females in Pithecia pithecia groups. The Witi Kreek trail. The heterogeneous habitats of the Browns- largest body of data on Pithecia group size comes from 21 berg may limit the distribution of a habitat specialist such as groups censused in Guyana, in which one group of 12 was Saimiri. For example, Peres (1997) reported high sighting seen (Lehman et al., 2001). If that outlier is removed, the rates of Saimiri in three várzea forests in Amazonia, and average from the remaining 20 groups is 4.4 ± 1.82 indi- their absence or relative rarity in 12 terra firma forests. viduals (range 2-9). Groups ranging from 6 to 9 have been Saimiri had the highest sighting rates of the eight species at documented from island habitats (Setz and Gaspar, 1997; 16 sites in Guyana surveyed by Lehman (2000). Norconk, 1996), but the body of evidence from Guyana and from our census (average 4.65 ± 1.66) suggests that Saguinus midas and Pithecia pithecia had the second highest small group size is typical for white-faced sakis (see Fig. 2). encounter rates at the Brownsberg. While Saguinus appears Lehman et al. (2001) found significant differences between to be well-dispersed on both slopes and plateau, Pithecia the sizes of groups in Venezuela and Suriname, and between was encountered more frequently on plateau trails (see groups in Guyana and Suriname. The Venezuela-Suriname Table 3). comparison should be excluded based on the lack of dis- persal ability on the island habitat in Venezuela, and the The Brownsberg primate population may be summarized Guyana and Suriname data now seem quite comparable. as follows:
The more frequent encounter rates of Alouatta at the 1) Alouatta seniculus and Saguinus midas were well-dispersed Brownsberg probably reflect both the relatively small in relatively small home ranges both on the plateau and on home ranges used by howlers and a ban on hunting pri- the slopes of the berg. mates in the immediate vicinity of the plateau. Alouatta sightings are much reduced at sites where hunting is rela- 2) The two pitheciins were encountered frequently. The tively severe (e.g., the terra firma forest in Amazonia cen- home ranges of Pithecia appear to be small (one was cal- sused by Peres, 1997; and the Río Tapiche sites suveyed by culated as 10.3 ha, on the basis of repeated sightings and Bennett et al., 2001) and more common where hunting territorial behavior associated with intertroop encounters). is prohibited (e.g., Nouragues, in Simmen et al., 2001). Chiropotes occurred in larger groups than have been ob- Hunting at the Brownsberg does occur in active mining served at any other site (including other Suriname sites) areas, and may be the cause of the relatively rare encoun- and are relatively wide-ranging, but more cohesive when ters of Ateles paniscus during our census, besides their traveling than Cebus olivaceus. Pithecia was observed more threatening/evasive behavior when encountered. Encoun- often on the plateau than the slopes, and Chiropotes was ter rates of Ateles in un-hunted sites such as Nouragues, seen more often on the slopes. Chiropotes fed extensively on French Guiana, were much higher than our Brownsberg Pouteria melanopoda (Sapotaceae) during the census period. estimates (Simmen et al., 2001). Alternatively, our low The distribution of that tree may have influenced its rang- encounter rates may have been due to a seasonal shortage ing patterns at the time of the census, but the rich diversity of fruit in the census area. of saki resources may help to explain both the large group 98 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 99
sizes of Chiropotes and the high density of Pithecia groups. Animal Interactions in a Neotropical Rainforest. Kluwer For example, Fitzgerald et al. (2002: Appendix G) reported Academic Publishers, London. 10 species of Licania (Chrysobalanaceae), four species of Defler, T. R. 1982. A comparison of intergroup behavior in Lecythis and five ofEschweilera (Lecythidaceae), and 12 spe- Cebus albifrons and C. apella. Primates 23: 385-392. cies of Pouteria (Sapotaceae). Defler, T. R. 2003. Primates de Colombia. Conservación Internacional, Bogotá, DC, Colombia. 3) The two capuchin species appear to be relatively rare at Fitzgerald, K. A. 2003. Utilizing ecological indicators to the site, and both species may have large home ranges. Only assist in the management of Brownsberg Natuurpark, one Cebus apella group was seen and we estimated three Suriname, South America. Unpublished thesis, C. olivaceus groups within the census area. The data were Washington State University, Seattle. too few to assess habitat preferences for the capuchins, but Fitzgerald, K. A., De Dijn, B. P. E. and Mitro, S. they appeared to range widely. 2002. Ecological research and monitoring program 2001 - 2006. STINASU (Stichting Natuurbehoud 4) Saimiri and Ateles also appear to be relatively rare. We Suriname) – Foundation for Nature Conservation in saw Saimiri only once, but our census route covered only a Suriname. Available in print or electronic form from small part of their potential range. Ateles were heard often,
community in relation to fruit supplies. In: Nouragues: the highest concentration of sawmills anywhere in Brazil- Dynamics and Plant-Animal Interactions in a Neotropical ian Amazonia. Today, timber is scarce in the region, and Rainforest, F. Bongers, P. Charles-Dominique, P.-M. the sawmills have been moved to new frontiers, although Forget and M. Théry (eds.), pp.89-101. Kluwer Academic Paragominas still remains an important commercial center Publishers, London. for the industry. Sussman, R. W. 2000. Primate Ecology and Social Structure, Vol. 2: New World Monkeys. Pearson Custom Publishing, The landscape around Paragominas today is a mosaic of Needham Heights, MA. agricultural land, pastures, logged and burned forest, and Terborgh, J. 1983. Five New World Primates: A Study small patches of primary forest which cover about 6% in Comparative Ecology. Princeton University Press, of the original area (Nepstad et al., 1999). The region of Princeton, NJ. Paragominas has undergone some of the most intense de- Wallace, R. B., Painter, R. L. E., Rumiz, D. I. and Taber, forestation and habitat degradation – and today supports A. B. 2000. Primate diversity, distribution and relative the highest human population density – of anywhere in the abundances in the Ríos Blanco y Negro Wildlife Reserve, Brazilian Amazon. Santa Cruz Department, Bolivia. Neotrop. Primates 8(1): 24-28. Although the remaining fragments suffer from hunting and selective logging, some still maintain primate populations (Lopes and Ferrari, 2000). In this study I evaluate the ef- PRIMATES IN A FOREST FRAGMENT IN EASTERN fects of this land use model on primates in a forest fragment AMAZONIA isolated since the late 1970s and composed of three differ- ent habitats (unlogged - UN, logged - LG and secondary Oswaldo de Carvalho Jr. forest - SF), and compare my results with other studies in the same region. Introduction Study Area Many new towns were established along the Belém-Brasí- lia Highway following its construction in the 1960s. One Data were collected at Fazenda Vitoria (FV) (02°55’S, was Paragominas, in the northeastern region of the state of 47°35’W), 6 km northwest from Paragominas town. Rain- Pará (Fig. 1). Large areas of forest in this region were cut fall (1750 mm/yr) varies seasonally, with a pronounced dry for cattle pasture during the 1970s; and due to the deple- season between July and November (< 50 mm/month) tion of timber resources in southern Brazil, in the 1980s (EMBRAPA-CPATU). Hunting pressure is high, and hunt- Paragominas also became an important logging center, with ers are frequently encountered, especially on weekends.
Figure 1. Location of the Fazenda Vitória (1) and the other sites in the state of Pará in eastern Brazilian Amazonia. See Table 1. 100 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 101
At the time of the study, there was a forest fragment on The primates observed during the census were Alouatta the FV of approximately 400 ha: 210 ha of primary forest belzebul belzebul, Chiropotes satanas satanas, Saguinus niger (UN), 70 ha of logged forest (LG) and 60 ha of an 18- and Saimiri sciureus. The night monkey (Aotus infulatus) year-old secondary forest (SF) surrounded by pasture. Since and brown capuchin monkey (Cebus apella apella) were not 1984, a combined team from the Amazonia Environmental recorded, although they are known to inhabit the site. The Research Institute (Instituto de Pesquisas Ambientais da highest sighting rates for Alouatta, Chiropotes and Saguinus Amâzonia – IPAM), the Woods Hole Research Center were in the primary (undisturbed) forest. Squirrel monkeys (WHRC), Woods Hole, MA, the Center for Research in were seen just once in secondary forest (Table 3). Agro-forestry in the Eastern Amazon (CPATU) of the Bra- zilian Agricultural and Cattle-Breeding Research Company Discussion (EMBRAPA) (Centro de Pesquisa Agroflorestal da Amazônia Oriental – CPATU/EMBRAPA) and the Federal University Six species inhabit the study area: four were confirmed by of Pará (UFPA) have conducted research on forest ecology actual sightings, and Cebus apella and Aotus infulatus were re- in one area of 260 ha (80 UN, 70 LG, 60 SF and 50 in ported by local people. The four species observed during the abandoned pasture). study were seen in each of three forest types (primary, logged and secondary forest). Although the sighting rate in dis- Methods turbed forest was lower than in primary, it has an important role for some species. For example, during a six-month study I used the Line Transect Method (NRC, 1981; Brockel- nearby, Oliveira and Ferrari (2000) observed S. niger using man and Ali, 1987) to evaluate the composition and disturbed forest for feeding, while primary forest provided abundance of the primate community. When a group their sleeping sites. Surprisingly, Cebus apella – generally one was sighted the following data were noted: date, time of of the commoner primates in Amazonia – occurs in very low day, trail, location on the trail, species identification, number densities at FV. The reasons for this are not known, but may of animals and animal-to-trail perpendicular distance. In reflect local ecological factors, such as forest type, composi- order to compare this study area with other sites (Table 1), tion and productivity, as well as human interference. I calculated the number of individuals sighted per 10 km (sighting rate) as suggested by Lopes and Ferrari (2000). The only species expected but not seen was Cebus kaapori. The Ka’apor capuchin has a restricted range, is rare, and The transects were walked between 06:00-12:00 and occurs at low densities (Ferrari and Lopes, 1996; Carvalho 16:00-18:00 at a mean speed of 1 km/h on a 4-km-long Jr. et al., 1999). Although Carvalho Jr. et al. (1999) sug- trail (2 km UN, 1 km in LG, and 1 km in SF). A total gested that the abundance of C. kaapori is inversely related of 69 km (23 km in each habitat) was surveyed during the to the presence and abundance of C. apella, at least at FV, late dry season to early wet season of 1994-1995. other factors may also be influencing its distribution there, such as intolerance to high levels of habitat degradation Results (Carvalho Jr. et al., 1999).
Eight mammal species were recorded in 40 sightings, 25 of In general, it would seem that FV maintains higher popu- which were of primates of four species. Sighting rates were lation densities of these primates when compared with 5.88/10 km walked for all mammals and 3.68/10 km for other sites (Table 2). In a rank of the sighting rates for primates. Each primate species was seen in all three habitat the 10 sites, the FV has the highest density of Saguinus types. Table 2 compares the sighting rates at FV with other niger, was second in this respect for Alouatta belzebul and sites in the same region (Fig. 1). For details on each site see Saimiri sciureus, and third for Chiropotes satanas. The Lopes and Ferrari (2000), Emídio-Silva (1998) and Boba- high sighting rates at FV might be a result of: 1) rapid dilla and Ferrari (1998). deforestation, which packed the primates into this frag-
Table 1. Characteristics of sites in eastern Amazonia used for comparison with the Fazenda Vitória, Paragominas.
Municipality Size (ha) Vegetation disturbance Hunting pressure Source Site 1 Paragominas 20,000 Moderate None 1 Site 2 Tailândia 18,000 Moderate High 2 Site 3 São Domingos do Capim 8,000 High High 2 Site 4 Irituia 5,000 Moderate Moderate 2 Site 5 Gurupí 340,000 Moderate to Low Low 2 Site 6 Novo Repartimento 350,000 Moderate to Low Moderate 3 Site 7 Novo Repartimento 350,000 Moderate to Low Moderate 3 Site 8 Novo Repartimento 7,000 Moderate to High Moderate 4 Site 9 Melgaço 300,000 Low Low 4 Sources: 1. Carvalho Jr. and Pinto, in prep.; 2. Lopes, 1993; 3. Emídio-Silva, 1998; 4. Bobadilla and Ferrari, 1998. 102 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 103
Table 2. Sighting Rate (SR) of primates at FV and other sites in the region. Number of sightings in parentheses. A. belzebul C. satanas S. midas S. sciureus Transect length (km) Source FV 1.32 (09) 0.44 (03) 1.76 (12) 0.14 (01) 69 This study Site 1 0.72 (05) 0.58 (07) 0.58 (03) – 69 1 Site 2 0.005 (01) 0.28 (06) 1.20 (26) – 216 2 Site 3 0.20 (04) 0.005 (01) 1.22 (25) – 205 2 Site 4 0.25 (10) 0.34 (14) 1.47 (60) – 408 2 Site 5 0.56 (27) 0.37 (18) 1.10 (53) 0.002 (01) 480 2 Site 6 0.31 (03) 0.52 (05) 0.10 (01) 0.10 (01) 96 3 Site 7 0.98 (08) 0.12 (01) 0.25 (02) – 81 3 Site 8 1.00 (10) 2.07 (21) 0.50 (05) 0.40 (04) 101 4 Site 9 2.08 (111) 0.11 (06) 1.11 (59) – 533 4 Sources: 1. Carvalho Jr. and Pinto, in prep.; 2. Lopes, 1993; 3. Emídio-Silva, 1998; 4. Bobadilla and Ferrari, 1998.
Table 3. Sighting Rate (SR) of primates at the Fazenda Vitória in the different habitats. Number of sightings in parentheses. A. belzebul C. satanas S. midas S. sciureus Primary Forest 2.61 (06) 0.87 (02) 2.61 (06) 0 Logged Forest 1.30 (03) 0.43 (01) 1.74 (04) 0 Secondary Forest 0 0 0.87 (02) 0.43 (01)
ment (in which case the population densities may decline References over the coming years); 2) Low hunting pressure on pri- mates in the region, except for howlers (Cymerys, 1994); Brockelman, W. Y. and Ali, R. 1987. Methods of survey- 3) Absence of potential predators (J. R. Martins, pers. ing and sampling forest primate populations. In: Primate comm.); and 4) ecological and behavioral flexibility of Conservation in the Tropical Rainforest, C. W. Marsh primate species. Other factors, such as interspecific com- and R. A. Mittermeier (eds.), pp.21-62. Alan R. Liss, petition and floristic composition of the forest fragments, New York. are also important influences on the occurrence and local Bobadilla, U. and Ferrari, S. F. 1998. First detailed data on abundance of primate species. Chiropotes satanas utahicki Hershkovitz, 1985. Neotrop. Primates 6(1): 17-18. There is only one strictly protected area in eastern Ama- Carvalho Jr., O., Pinto, A. C. B. and Galetti, M. 1999. New zonia, the Gurupí Biological Reserve; it is seriously threat- observations on Cebus kaapori Queiroz, 1992, in eastern ened, however, and much of its forest has already been de- Brazilian Amazonia. Neotrop. Primates 7(2): 41-43. stroyed. Numerous logging companies are active there and Cymerys, M. 1994. Sustainable faunal harvest: Game man- causing widespread environmental degradation through agement for small-landholders in eastern Amazonia. Un- pollution and hunting, resulting in threats to many species published report, Woods Hole Research Center, Woods of the region. East of the Rio Tocantins, A. belzebul ululata Hole, MA, and Universidade Federal do Pará, Belém. (coast of Maranhão) and Cebus kaapori are now considered Emídio-Silva, C. E. 1998. A caça de subsistência praticada Critically Endangered, and Chiropotes satanas satanas En- pelos índios Parakanã (sudeste do Pará): Características e dangered (Rylands and Chiarello, 2003). With such threats sustentabilidade. Master’s thesis, Universidade Federal do increasing, these relatively small forest fragments – together Pará, Belém. with the few large remaining areas of undisturbed forest Ferrari, S. F. and Lopes, M. A. 1996. Primate populations in – could play an important role in conservation strategies eastern Amazonia. In: Adaptive Radiations of Neotropical in the future. Primates, M. A. Norconk, A. L. Rosenberger and P. A. Garber (eds.), pp. 53-67. Plenum Press, New York. Acknowledgements: Fieldwork was supported by grants Lopes, M. A. and Ferrari, S. F. 2000. Effects of human colo- from USAID and the Federal University of Pará (UFPA), nization on the abundance and diversity of mammals in Belém. Thanks to A. C. M. Oliveira and C. Emídio-Silva eastern Amazonia. Conserv. Biol. 14: 1658-1665. for helping me to collect field data, and to IPAM for lo- Nepstad, D. C., Moreira, A. G. and Alencar, A. A. 1999. gistical support. S. F. Ferrari made helpful comments on A Floresta em Chamas: Origens, Impactos e Prevenção de the manuscript. Fogo na Amazônia. Programa Piloto para a Proteção das Florestas Tropicais do Brasil, Brasília. Oswaldo de Carvalho Jr., Instituto de Pesquisa Ambiental NRC. 1981. Techniques for the Study of Primate Population da Amazônia (IPAM), Avenida Nazaré 669, 66035-170 Ecology. National Research Council (NRC), National Belém, Pará, Brazil. E-mail:
Oliveira, A. C. M. and Ferrari, S. F. 2000. Seed dispersal juvenile male Químico then approached and examined it, by black-handed tamarins, Saguinus midas niger (Cal- but soon went away, following the group and leaving the litrichinae, Primates): Implications for the regeneration rat on the ground. of degraded forest habitats in eastern Amazonia. J. Trop. Ecol. 16: 709-716. On examination, most of the muscle tissue of the carcass Rylands, A. B. and Chiarello, A. G. 2003. Official List of was intact, except for the abdominal layers and the face Brazilian Fauna Threatened with Extinction – 2003. Neo- muscles. The rat’s belly was ripped open, and its liver, pan- trop. Primates 11(1): 43-49. creas, stomach, heart, the entire digestive tract, and the brain were completely eaten. Consumption of the head and brains of small vertebrate prey has also been regis- SOME OBSERVATIONS ON THE PREDATION OF SMALL tered by Heymann et al. (2000) in their study of Saguinus MAMMALS BY TUFTED CAPUCHIN MONKEYS (CEBUS mystax and Saguinus fuscicollis. Biting the head of lizards, APELLA) frogs and bird nestlings was seen as a killing strategy with a rich energy source, the brain, as a reward. Izawa (1978) Briseida D. Resende, Vivian L. G. Greco described Cebus apella in Colombia which killed frogs by Eduardo B. Ottoni, Patrícia Izar squeezing the prey’s neck or biting them, and then con- suming the thighs, the tips of the hands and feet, and the Capuchin monkeys are the most omnivorous of the New viscera. We were unable to see the way the prey was killed, World primates and are predators of small vertebrates (Ter- but the monkeys certainly showed a preference for eating borgh, 1983). Cebus capucinus has been observed hunting the intestines and brain. Later that morning, at 1135, coatis (Nasua narica) and squirrels (Sciurus variegatoides) in VG observed an adult male eating a small young, pink Costa Rica (Newcomer and De Farcy, 1985; Rose, 1997). mammal around 5 cm in length. Another adult male had Brown capuchin monkeys (Cebus apella) capture and eat liz- also been observed eating two young mammals similar to ards, squirrels, frogs and birds (Izawa, 1978; Terborgh, 1983; this one in July 2002. Galetti, 1990). Ferreira et al. (2002) described predation on birds by a group of tufted capuchins at the Tietê Ecological On 27 May, 2003, at 0945, VG observed an adult female Park, São Paulo. Here we report on our observations of this carrying the carcass of an opossum infant (Didelphis sp). same, semi-free-ranging group eating small mammals. The The dominant male, Bisqüi, and another adult female were group lives in an 18 ha reforested area in the Tietê Ecologi- nearby. Almost the entire carcass was consumed; only the cal Park, São Paulo, Brazil. A detailed description of the area head, skin and bones and a small part of the intestines re- and the group is given by Ottoni and Mannu (2000). mained. Unlike the rat carcass, in this case the muscle tissue was broadly consumed and the brain was intact. On 6 June, 2001, at around 0930, one of us (BDR) was following the capuchin group and saw the juvenile male Although the capuchin monkeys are provisioned daily, Frank eating birdseed near the juvenile male Lobato they forage continuously, eating fruits, leaves, birds and and juvenile female Vavá. Suddenly he descended to the invertebrates such as spiders and worms (Ferreira et al., ground, grabbed a mouse hidden in the bushes and took it 2002). As opportunists, they probably capture vertebrate to a tree. The mouse was not seen moving prior to capture, prey whenever possible, even though food scarcity is not a so we cannot be sure if he had killed it or if it was already problem for this group; varied protein sources are always dead. Frank examined its belly and ripped the skin between welcome, and hunting behaviors may be rewarding per se. the hind limbs, but soon abandoned the prey. Lobato ap- In contrast to what was observed with Izawa’s group in proached, took the mouse and, after a brief examination, also abandoned it.
On 15 March, 2003, at around 1050 in the morning, BDR and VG observed the dominant male Bisqüi on a branch, 10 m above the ground, eating the head and intes- tines of an adult male rat (Rattus rattus). The adult female Cisca, carrying her 5-month-old infant, and the adult male Medeiros were watching Bisqüi from very close by. An unidentified immature was also nearby, and watching keenly. Bisqüi showed great tolerance, never threatening or attacking those who were watching. The unidentified immature was able to eat a piece of the viscera. After about three minutes, Bisqüi abandoned the rat, which fell on the ground. Female juvenile Ada went down and took the car- cass. We observed her from a close distance (around 4 m). She ate parts of the digestive tract, liver and pancreas, and Figure 1. Adult female (Cisca) observes dominant male (Bisqüi) after about four minutes, also abandoned the carcass. The eating a rat. 104 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 105
Colombia, in all predation events described here the pos- Rose, L. 1997. Vertebrate predation and food-sharing in sessor tolerated the proximity of conspecifics; this created Cebus and Pan. Int. J. Primatol. 18: 727-765. opportunities for food transfer, either direct and tolerated Terborgh, J. 1983. Five New World Primates. Princeton or, more often, through scrounging. Food transfer in this University Press, Princeton, NJ. group was also registered in bird predation events, and scrounging was also the most common type of transfer (Ferreira et al., 2002). INSECT-EATING BY SPIDER MONKEYS
In a review of the genus by Freese and Oppenheimer Andres Link (1981), vertebrate prey listed included only lizards, birds and rodents in the diet of C. capucinus, and frogs in the diet Introduction of C. apella. While John Oppenheimer was the pioneer in studies of this genus in the wild (C. capucinus in particular), Studies on the diet and feeding behavior of spider monkeys this diet list reflected the paucity of information available (Ateles spp.) have revealed they are primarily frugivorous, at the time. As new field studies are conducted, our under- with fruits representing between 72% and 90% of their standing of the diversity of prey taken by tufted capuchins, diet (Carpenter, 1935; Hladik and Hladik, 1969; Klein and the dynamics of food transfer among them, will con- and Klein, 1977; Van Roosmalen, 1985; Chapman, 1987; tinue to improve. Symington, 1988; Dew, 2001). Flowers and young leaves are also eaten frequently, especially when fruit is scarce (Van Acknowledgements: We thank the staff of the Tietê Ecologi- Roosmalen and Klein, 1988; Castellanos, 1995; Nunes, cal Park for their support, and also Michele Verderane and 1998; Stevenson et al., 2000). Bark, decaying wood, fungus, Guilherme Imura, who helped in the description of the seeds, soil from salt-licks and termite nests, insects and other predation on the infant opossum. This work was funded by items are seldom consumed and represent only a small part a grant from the Fundação de Amparo à Pesquisa do Estado of their diet (see Van Roosmalen and Klein, 1988). de São Paulo – FAPESP (São Paulo State Research Support Foundation) (Process 99/11573-2). Insect-eating in spider monkeys has been reported in several studies and, except for passive consumption (for Briseida D. Resende, Vivian L. G. Greco, Eduardo B. example, fig wasps in fig fruits), it represents a minor part Ottoni and Patrícia Izar, Departamento de Psicologia of their feeding activities. Wagner (1956) reported that Experimental, Instituto de Psicologia, Universidade de São spider monkeys eat insects and insect larvae. Termites are Paulo, Avenida Prof. Mello Moraes 1721, São Paulo 05508- eaten selectively (Klein and Klein, 1977; Van Roosmalen, 030, São Paulo, Brazil. E-mail:
between the eastern Andes and the Serranía de La Macare- from their tails in front of the bee nest, or sat on the trunk na, Departamento de Meta, Colombia (2°40’N, 74°10’W; and branches nearby waiting for their turn to gain access. 350-400 m a.s.l.). Annual temperature is relatively constant When bees attacked and flew into the monkey’s fur, they at approximately 26°C and rainfall is highly seasonal, with were easily captured and eaten. Mothers ate simultaneously a dry season between December and March and the rainy with their juveniles and infants, capturing bees on their season between April and November. Peak rainfall is in own or another individual’s fur. When the bees stopped June and July, and the region averages 2700 mm annually attacking, the spider monkeys would disturb the nest with (Kimura et al., 1994; Stevenson, 2002). their hands, and the bees would start attacking again. The feeding bouts lasted 2, 4, 5, 6, 6, 7, 11 and 13 minutes, and Field Methods average feeding rates were 18.0 ± 6.2 bees/min (SD), range 12-30 (n = 9). These few observations reveal that spider Observations of insect-eating by white-bellied spider mon- monkeys could be eating a large quantity of bees per feed- keys were recorded during 13 months of fieldwork, from ing bout, and although data were only collected from focal January 2001 to January 2002. Focal animal sampling (Alt- animals, several spider monkeys fed on these nests after and mann, 1974) was used to study their basic ecology and diet. before the focal animal started its feeding bout. Instantaneous sampling (every five minutes) was used to quantify activity budgets and habitat use. Continuous sam- Caterpillars were eaten intensively during a short period of pling was used every time the focal animal began to feed. the year in October, as well as on one occasion in February, Total feeding time per bout, the species and item eaten, and when a medium size (c. 30-40 mm long) caterpillar was DBH (diameter at breast height) in trees and lianas were eaten by a female with twins. The other five caterpillar- recorded, in addition to the number of individuals feeding eating bouts were observed during focal animal sampling; on the same item and, when possible, consumption rates in each case the spider monkeys ate caterpillars of a single (measured in number of ingested items per minute). species, which were heavily clumped in the leaves of a few individual trees. During October almost 9% of the feeding Results time of spider monkeys was invested in this item, which was the fourth most commonly eaten item during that month. Sixteen insect-eating bouts were observed during the study, One to three monkeys were seen eating caterpillars in the during which the spider monkeys ate orthopterans (n = 2), same tree. Each individual actively foraged for and captured meliponid bees (n = 8) and lepidopteran larvae (n = 6). Fif- the caterpillars by directly licking or biting the fresh or dry teen of these bouts were observed directly, while one event leaves. These five feeding bouts lasted 1, 17, 27, 11 and 53 was inferred by insect exoskeletons found in fecal samples. min. No feeding rates were obtained due to the difficulty Grasshoppers (Orthoptera) were probably eaten opportu- in recording when a single caterpillar had been ingested, nistically. Caterpillars and bees were eaten intensively, and but large quantities of caterpillars were consumed at each active foraging to obtain these food items was observed in feeding bout. all of these feeding bouts. Discussion Insect-eating constituted 1.5% of the total feeding time during the study year. All age/sex classes were seen eating Insect-eating by spider monkeys is uncommon, but may insects and, although no aggression was seen on these occa- reveal some important aspects of their feeding ecology sions, there were some displacements at the meliponid bee and adaptations. The few species of insects eaten are the nests. Spider monkeys were observed eating grasshoppers only animal matter in their otherwise plant-supported twice: in February, I collected two fecal samples next to each diets. In several studies carried out on different species of other, each of which contained one-half of the exoskeleton spider monkeys, caterpillars were the only group of insects of an orthopteran (c. 40 mm long); and in April, one small observed in the diet of this genus. In all of these studies, grasshopper was caught from the top of a leaf and eaten by this activity occurred in specific short periods (c. 15 days) a female with an infant (J. Cajiao, pers. obs.). of the year (Van Roosmalen, 1985; Chapman, 1987; Symington, 1988; this study), probably when the cater- Meliponid bees (Scaptotrigona sp.) were also part of the pillars of some lepidopteran species hatch and aggregate diet of this spider monkey group. Bee-eating was seen on the leaves of particular trees. These caterpillars were repeatedly throughout the year, and although it is an in- eaten only in a short period of the year, which is similar frequent activity (compared to eating fruits or leaves), large to the availability of other food items such as some fruits, quantities of bees were eaten on each occasion. Six out of flowers and leaves of particular plant species (in contrast eight observations were at the same two bee nests located with meliponid bees, which were available throughout the on the trunk of an emergent Bombacopsis quinata (Jacq.) year). Taxonomic identification of these caterpillars, and Dugang (Bombacaceae) tree, another nest was in another those eaten at other sites, would be useful to determine if B. quinata tree, and one in an unidentified tree. All were in they are phylogenetically related, and whether they might the canopy, about 20-25 m above the ground. One to three have been part of the diet of an ancestral spider monkey, or monkeys were seen eating bees simultaneously at the same if the exploitation of this food resource has evolved sepa- nest (excluding dependant infants). They usually hung rately in isolated populations. 106 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 107
Meliponid bees were eaten at different times of the year, and woolly monkeys (Lagothrix spp.); these genera overlap and this is the first report on such repeated feeding bouts widely in their geographic distribution, and are sympatric at at bee nests. In these cases, the spatial and temporal several northwestern Amazonian sites in Ecuador and Co- availability of bees is predictable and somewhat constant lombia (see Strier, 1992; Stevenson et al., 2000; Dew, 2001). throughout the year. Nevertheless, the spider monkeys ate Differences in their diets include the higher proportion of them on only a few occasions, and this feeding source was lipid-rich fruits eaten by spider monkeys, and the more fre- totally ignored at other times, even though they rested or quent foraging and insect-eating by woolly monkeys. passed very close to the nests, and bees were seen flying around them. It would seem that fruit availability is not an Differences in the diets of the atelines are apparent in the important determinant of this behavior, as bees were eaten proportions of food items they consume, which probably during periods of fruit abundance and scarcity alike (Link, evolved to avoid direct competition. Although all are fru- unpubl. data). givorous, each species complements its diet with different items. Howler monkeys (Alouatta spp.) eat a great variety of Insect-eating by spider monkeys, and its selectivity and mature and young leaves, as well as other vegetative plant possible consequences, are still not well understood. There parts (Neville et al., 1988; Juliot and Sabatier, 1993) and are few data available, and practically no information on there is also limited evidence of insect-eating. Woolly mon- the taxonomic groups eaten or on their nutritional compo- keys eat young leaves and insects, especially in periods of nents. Most studies of primate diets focus on quantitative fruit scarcity (Ramirez, 1988; Defler and Defler, 1996; Ste- and qualitative analysis of the major food items. Consid- venson et al., 1994). Ateles and muriquis (Brachyteles spp.) erable information of this sort is now available for several base their diet on fruits and leaves, but the former relies species of spider monkeys at different localities (Carpenter, more on fruits, while the latter feeds more on leaves (Van 1935; Hladik and Hladik, 1969; Klein and Klein, 1977; Roosmalen and Klein, 1988; Nishimura et al., 1988; Strier, Van Roosmalen, 1985; Chapman, 1987; Symington, 1987; 1991; Nunes, 1998). Both spider and howler monkeys Van Roosmalen and Klein, 1988; Cant, 1990; Castellanos, include small proportions of selected insects in their diet 1995; Nunes, 1998; Wallace, 1998; Dew, 2001). It is pos- (Milton, 1980; references above) and more information is sible that food items such as insects, which are only a small needed to understand why they do not rely on other insects, part of their diet, contribute essential or complementary as woolly monkeys do, in order to complement their nutri- nutrients, besides the soil eaten by both howler and spider tional requirements, considering the widespread availability monkeys at salt-licks (see Izawa, 1993). of this resource in the forest (Izawa, 1993).
One important aspect of the feeding ecology of spider mon- Acknowledgements: I thank G. de Luna and J. Cajiao for keys that has not been studied in detail is the set of physical their support and data collection in the field. C. Chap- constraints they experience while capturing, manipulating man, K. Izawa, P. Stevenson, H. Castellanos and G. de and exploring objects with their hands. Their thumbless Luna provided useful comments on the manuscript. hands make them less agile at such foraging when compared G. Nates (Universidad Nacional de Colombia) helped with the with other genera such as Saimiri, Cebus or Lagothrix. This identification of the insects eaten byAteles in our study site. is supported by the fact that other primate groups which G. de Luna, N. Silva, A. Sanabria and B. Ramírez helped in have vestigial or absent thumbs (i.e., Colobus spp.) rarely collecting the insects. Members of the Unidad Administra- include insects in their diets (see Davies and Oates, 1994). tiva Especial del Sistema de Parques Naturales Nacionales Thumbless hands and long fingers are adaptations that are de Colombia collaborated with this research at Tinigua probably associated with their locomotive patterns and a National Park. Finally, I thank the Colombian-Japan agree- diet based on fruits and leaves, which certainly constrains ment through K. Izawa and C. Mejía, who provided per- their ability to capture fast-moving animal prey. mission for this research at the CIEM.
Given the “precision-grip” constraints on the spider monkey Andres Link, Doctoral Program in Physical Anthropol- hand, the caterpillars and meliponid bees which were eaten ogy at New York University, Rufus D. Smith Hall, 25 in Tinigua Park might represent a food resource which does Waverly Place, New York, NY 10003, USA. E-mail: not require high energetic costs in foraging and capturing.
forest, southern Venezuela. Doctoral dissertation, The Stevenson, P. R., Quiñones, M. J. and Ahumada, J. 1994. Eco- University of Exeter, Devon, UK. logical strategies of woolly monkeys (Lagothrix lagothricha) at Chapman, C. A. 1987. Flexibility in diets of three species of La Macarena, Colombia. Am. J. Primatol. 32: 123-140. Costa Rican primates. Folia Primatol. 49: 90-105. Stevenson, P. R., Quiñones, M. J. and Ahumada, J. 2000. Davies, A. G. and Oates, J. F. (eds.). 1994. Colobine Mon- Influence of fruit availability on ecological overlap among keys: Their Ecology, Behaviour and Evolution. Cambridge four Neotropical primates at Tinigua National Park, Co- University Press, Cambridge. lombia. Biotropica 32: 533-544. Defler, T. R. and Defler, S. B. 1996. Diet of a group of Strier, K. B. 1991. Diet in one group of woolly spider Lagothrix lagothricha lagothricha in southeastern Colom- monkeys, or muriquis (Brachyteles arachnoides). Am. J. bia. Int. J. Primatol. 17: 161-189. Primatol. 23: 113-126. Dew, J. L. 2001. Synecology and seed dispersal in woolly Strier, K. B. 1992. Atelinae adaptations: Behavioral strate- monkeys (Lagothrix lagothricha poeppigii) and spider gies and ecological constraints. Am. J. Phys. Anthropol. 88: monkeys (Ateles belzebuth belzebuth) in Parque Nacional 515-524. Yasuní, Ecuador. Doctoral dissertation, University of Symington, M. M. 1988. Demography, ranging patterns California, Davis, CA. and activity budgets of black spider monkeys (Ateles Hladik, A. and Hladik, C. M. 1969. Rapports trophiques paniscus chamek) in the Manu National Park, Peru. Am. entre végétation et primates dans la forêt de Barro Colo- J. Primatol. 15: 45-67. rado (Panama). La Terre et la Vie 23: 25-117. Van Roosmalen, M. G. M. 1985. Habitat preference, diet, Izawa, K. 1993. Soil-eating by Alouatta and Ateles. Int. J. feeding behavior and social organization of the black Primatol. 14: 229-242. spider monkey, Ateles paniscus paniscus, in Surinam. Acta Julliot, C. and Sabatier, D. 1993. Diet of the red howler Amazonica 15: 1-238. monkey (Alouatta seniculus) in French Guiana. Int. J. Van Roosmalen, M. G. M. and Klein, L. L. 1988. The Primatol. 14: 527-550. spider monkeys, genus Ateles. In: Ecology and Behavior of Kimura, K., Nishimura, A., Izawa, K. and Mejía, C. 1994. Neotropical Primates, Vol. 2, R. A. Mittermeier, A. B. Ry- Annual changes of rainfall and temperature in a tropical lands, A. F. Coimbra-Filho and G. A. B. da Fonseca (eds.), seasonal forest at La Macarena field station, Colombia. pp.455-537. World Wildlife Fund, Washington, DC. Field Studies of New World Monkeys La Macarena Colom- Wagner, H. O. 1956. Freidlandbeobachtungen an Klam- bia 9: 1-3. meraffen. Zeit. für Tierpsychol. 13: 302-313. Klein, L. L. and Klein, D. J. 1977. Feeding behavior of the Wallace, R. B. 1998. The behavioral ecology of black spider Colombian spider monkey. In: Primate Ecology, T. H. Clut- monkeys in north-eastern Bolivia. Doctoral dissertation, ton-Brock (ed.), pp.153-181. Academic Press, London. University of Liverpool, Liverpool, UK. Milton, K. 1980. The Foraging Strategy of Howler Monkeys: A Study in Primate Economics. Columbia University Press, New York. LAGOTHRIX LAGOTHRICHA OR LAGOTHRIX Neville, M. K., Glander, K. E., Braza, F. and Rylands, A. B. LAGOTRICHA: WHICH IS IT? 1988. The howling monkeys, genus Alouatta. In: Ecology and Behavior of Neotropical Primates, Vol. 2, R. A. Mit- Thomas R. Defler termeier, A. B. Rylands, A. F. Coimbra-Filho and G. A. B. da Fonseca (eds.), pp.349-453. World Wildlife Fund, When von Humboldt (1812) wrote the holotypic descrip- Washington, DC. tion of Humboldt’s woolly monkey, he spelled the species Nishimura, A., Fonseca, G. A. B. da, Mittermeier, R. A., name both lagotricha and lagothricha. According to some, Young, A. L., Strier, K. B. and Valle, C. M. C. 1988. lagothricha (and its variant lagothrica) are incorrect Latiniza- The muriqui, genus Brachyteles. In: Ecology and Behav- tions of the Greek words λἁγο(Ϛ) - lago(s) (hare) + θρἱχο(Ϛ) ior of Neotropical Primates, Vol. 2, R. A. Mittermeier, - thrico(s) (hair)1 because of the preceding vowel, o, which A. B. Rylands, A. F. Coimbra-Filho and G. A. B. da would require the form “trichos” rather than “thrichos”. The Fonseca (eds.), pp.577-610. World Wildlife Fund, Wash- use of the two versions was certainly a lapsus on von Hum- ington, DC. boldt’s part. However, when revising the genus, Fooden Nunes, A. 1998. Diet and feeding ecology of Ateles belze- (1963), under Article 24 (24.2) of the International Code of buth belzebuth at Maracá Ecological Station, Roraima, Zoological Nomenclature, chose the variation lagothricha as Brazil. Folia Primatol. 69: 61-76. the “correct legal spelling” for Lagothrix lagothricha. Ramírez, M. 1988. The woolly monkeys, genus Lagothrix. In: Ecology and Behavior of Neotropical Primates, Vol. 2, “Article 24: Precedence between simultaneously published R. A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho names, spellings or acts. and G. A. B. da Fonseca (eds.), pp.539-575. World Wild- life Fund, Washington, DC. 24.1. Automatic determination of precedence of Stevenson, P. R. 2002. Frugivory and seed dispersal by names. When homonyms or synonyms are established woolly monkeys at Tinigua National Park, Colombia. Doctoral dissertation, State University of New York, Stony Brook. 1 No pun intended, as von Humboldt was writing in French, not English. 108 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 109
simultaneously, but proposed at different ranks, in the of mtDNA from individuals of the two taxa lagothricha and family group, genus group or species group the name lugens, but in the same study they found different haplo- proposed at higher rank takes precedence [Arts. 55.5, types of mtDNA in Saimiri sciureus albigena and Saimiri 56.3, 57.7]. See Article 61.2.1 for the precedence of sciureus macrodon, suggesting that we need yet more molecu- simultaneous but different type fixations for taxa and lar information to be able to truly solve the species problem their nominotypical subordinate taxa. in Lagothrix. A difference in haplotypes alone is insufficient for the establishment of a new species name. 24.2. Determination by the First Reviser. Thomas R. Defler, Instituto Amazónico de Investigaciones, 24.2.1. Statement of the Principle of the First Re- Universidad Nacional de Colombia, A. A. 215, Leticia, Am- viser. When the precedence between names of nomen- azonas, Colombia. E-mail:
Brazilian zoos (see “Acknowledgements”). It was not pos- BIRTHS OF ALOUATTA CARAYA AND A. BELZEBUL sible to test the data on A. belzebul for seasonality because (ATELIDAE, ALOUATTINAE) IN CAPTIVITY IN BRAZIL of the small sample. (Data on the reproduction of this spe- cies at the National Primate Center [Kingston, 1987] were Daniela Fichtner Gomes not available for this research.) Although A. belzebul birth Júlio César Bicca-Marques records were scattered throughout the year, most of them (78%) occurred between September and February (Fig. 1). The genus Alouatta (howler monkeys) has the largest geographic distribution of all Neotropical primate genera, Data on A. caraya were grouped (January-February, occurring from Mexico to Argentina and Brazil (Neville March-April, and so on) for statistical analysis because of et al., 1988). Its ecology and behavior have been a recurrent the low frequency of birth records per month. There was topic of field research, but very few studies have been con- no evidence of seasonality, since birth records were well ducted in captivity due to the difficulty of keeping these distributed across the year (χ² = 4.75, df = 5, NS; Fig. 1). primates outside of their natural environment (Kinzey, The analysis of birth records of A. caraya at 25 zoos in the 1997). The species A. caraya and especially A. belzebul are USA (compiled by LaHue, 2000) corroborates the absence still poorly known. of seasonal reproduction of this species in captivity (χ² = 11.02, df = 11, NS; Fig. 2). This research confirms results Alouatta caraya and A. belzebul live in social groups com- from other studies that suggest that A. caraya may give birth posed of two to 19 individuals. Generally, there are more throughout the year under the conditions of regular food adult females than adult males in the group (see Crockett availability observed in captivity (Shoemaker, 1979, 1982). and Eisenberg, 1987; Rowe, 1996). In A. caraya, sexual maturity is reached around 35-42 months in females and Acknowledgements: We thank the Pontifícia Universidade 24-37 months in males (Shoemaker, 1982). The menstrual Católica do Rio Grande do Sul for logistical support cycle in this species lasts on average 20 days (Colillas and and the zoos that kindly provided data for this research: Coppo, 1978). Estimates of the gestation period range from Parque Zoológico de Sapucaia do Sul/RS, Parque Balneário 152 to 195 days (see Calegaro-Marques and Bicca-Marques, Turístico Oásis/RS, Criadouro de Animais Silvestres da 1993), whereas the interbirth interval varies from seven to ITAIPU Binacional/PR, Zoológico de Curitiba/PR, Centro 27 months (Calegaro-Marques and Bicca-Marques, 1993; de Conservação da Fauna Silvestre de Ilha Solteira/SP, Lindbergh, 1978; Shoemaker, 1982; Zunino, 1996). Parque Zoológico Municipal “Quinzinho de Barros”/SP, Zoológico Municipal de Mogi Mirim/SP, Fundação Rio- Howler monkeys rarely breed in captivity, but some success Zoo/RJ, Fundação Zoobotânica do Distrito Federal/DF, has been achieved with Alouatta caraya (see Crockett, 1998; Kinzey, 1997). Studies of A. caraya suggest the absence of reproductive seasonality in captivity (Colillas and Coppo, 1978; LaHue, 2000; Lindbergh, 1978; Shoemaker, 1979, 1982), although conflicting results have been obtained in the wild (Zunino, 1996; see also Calegaro-Marques and Bicca-Marques, 1993; evidence of birth seasonality in wild A. palliata, A. pigra and A. seniculus is presented by Brockett et al., 2000; Crockett and Rudran, 1987; Fedigan et al., 1998; and Jones, 1980). According to Di Bitetti and Janson (2000), folivorous and large-sized Neotropical pri- mates such as Alouatta tend to be non-seasonal breeders. In Argentina, however, Zunino (1996) observed a greater frequency of births during the dry season, a time of higher availability of new leaves and fruits. He related this birth Figure 1. Monthly distribution of birth records of A. caraya (N = seasonality to three environmental variables: Temperature, 48) and A. belzebul (N = 9) at Brazilian zoos. rainfall, and especially food availability (Zunino, 1996).
Here we examine whether A. caraya and A. belzebul breed seasonally in captivity in Brazil based on an analysis of the monthly distribution of birth records. Data were obtained through a questionnaire sent to Brazilian zoos. The follow- ing information was requested: Species (scientific name), date of birth, litter size, sex of offspring, and characteristics of the cage (indoor/outdoor). Figure 2. Monthly distribution of birth records of A. caraya in A total of 48 births of A. caraya and nine of A. belzebul captivity in the U.S.A. (N = 280) (data compiled by LaHue, were recorded from 1960 to 2003 in outdoor cages at 12 2000). 110 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 111
Parque Zoológico de Goiânia/GO, Parque Zoobotânico de B. da Fonseca (eds.), pp. 349-453. World Wildlife Fund Carajás/PA and Museu Paraense Emílio Goeldi/PA. (WWF), Washington, DC. Rowe, N. 1996. The Pictorial Guide to the Living Primates. Daniela Fichtner Gomes and Júlio César Bicca-Marques, Pogonias Press, New York. Faculdade de Biociências, Pontifícia Universidade Católica Shoemaker, A. H. 1979. Reproduction and development do Rio Grande do Sul, Avenida Ipiranga 6681, Pd. 12A, of the black howler monkey Alouatta caraya at Columbia Porto Alegre 90619-900, Rio Grande do Sul, Brazil. Zoo. Int. Zoo Yrbk. 19: 150-155. E-mail:
triplets was stillborn; a second survived only one day with the first day, there is a four-hour break in feeding during its parents. We found the third neonate with low body the night, and with normal development, the interval temperature, an uncut umbilical cord, and shallow res- increases to six hours after one week of life. After ap- piration. The newborn cotton-top tamarins were slightly proximately 10 days, the intervals between the feedings injured, as immediately after birth their mother dropped are extended to three hours during the day. After 15 to 20 and bit them. days, depending upon the individual, the infant gradually receives solid food. Normally, the infants determine when Schröpel (1988a) wrote in detail about methods for hand- they will begin to eat solid food by showing interest in rearing cotton-top tamarins. From the first day of life, all of the human parent’s mouth and the chewing motion. In the hand-reared callitrichids are carried close to the body a natural rearing, infants regularly steal food from their of the “human parent” – usually on a piece of fur that has father’s mouth. In hand-rearing, the infant callitrichids been wrapped around the human parent’s arm. (At one receive banana pulp, apple pulp, and biscuit as the first time, the newborn cotton-top tamarins were put in a heat- solid foods with other foods introduced gradually. By ap- ing box during the first days of their life.) While clinging proximately 10 weeks there are longer intervals between to the “fur” of the human parent, the infant callitrichid formula feedings. experiences movements of the keeper similar to the natural movement of its parents. This supports the development of During hand-rearing the infants are weighed daily. Usually their sensory perception, communication and social behav- the daily weighing ends when the subjects reach between iour. However, if the subject is placed in a rearing-box when 80 and 100 days, because the young callitrichids become removed from its parents, this support is unavailable, and too agile, and the measurements are not exact. The birth there is the danger that “Kaspar Hauser Syndrome” may de- weights of the cotton-top tamarins were 47 g and 48 g velop. In my opinion, the rearing method we implemented (both males from a twin birth) and 40 g (female from a is important, even essential to achieve a normal social on- triplet birth). The two male golden-handed tamarins (from togenesis in young primates, because infant primates are separate twin births) weighed 41 g and 53 g. The male carried all the time by their mother or father (Schröpel, golden lion tamarin (from a triplet birth) weighed 65 g, 1982). There is a difference in the rearing of nesting mam- and the newborn common marmosets weighed between mals. Indeed, some keepers are also using the method of 20 g and 28 g. “parking” in the hand-rearing of primates. In most cases, we reintegrate the young hand-reared callitrichids into the The development of the total body weights for these four family group after three months, with a high rate of success. species of hand-reared callitrichids is shown in Figure 1a. In the meantime, some of the hand-reared subjects have The weight curves on the diagram increase in a gradually become parents themselves and have successfully reared linear fashion until the subjects reach 90 days of age. The their own infants. increase in the curves is shallower, however, in the first two weeks of life. The hand-reared Saguinus midas and Initially, the newborn callitrichids are bottle-fed every two Leontopithecus rosalia demonstrate a sine-like progress (less hours with a human infant milk formula; the quantity is pronounced in Leontopithecus) with slow growth at the be- dependent upon the newborn’s need. In the first days of ginning, more rapid growth between three and 10 weeks, life the quantity consumed is hardly measurable. From and finally slow growth again.
Figure 1. (a) Absolute weight development of Callithrix jacchus, Saguinus oedipus, Saguinus midas, and Leontopithecus rosalia. (b) Absolute weight gain of the callitrichids studied, presented as a regression line. S. oedipus, S. midas, and L. rosalia gain weight in the same scale, C. jacchus slightly less. 112 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 113
Kirkwood (1985) reported the weight development of callitrichids as a simple exponential curve with a flatten- ing gradient. In our current results we will proceed on the assumption that a gradual linear increase is generally typical in the first three months of life. If the weight gain of the individuals from each species is averaged over the first three months, then the common marmosets gain their body weight by 1.43 g daily; the golden-handed tamarins and the cotton-top tamarins by 1.95 g and 1.89 g per day, respectively; and the golden lion tamarin by 1.86 g daily. The tamarins and the lion tamarin are not notably different in their absolute weight increase (Fig. 1b).
It was noticeable while recording the weight measurements that the various species doubled their birth weight at differ- ent times while undergoing the same regimen of artificial Figure 2. Regression lines of the weight development on a rearing. In C. jacchus the birth weight doubled between percentage basis to the birth weight. days 18 and 26, in S. oedipus between days 27 and 28, in S. midas at days 32 and 35, and in L. rosalia at day 42. To compare the weight development among the species we computed the daily weight increase on a percentage basis of the birth weight (Fig. 2). There is a significant negative correlation between birth weight and weight development on a percentage basis (p < 0.05 to p < 0.001). Only be- tween S. midas and S. oedipus is the difference not signifi- cant; however, the birth weight of both these species differs only minimally. The birth weight of C. jacchus increased by 6.11% daily, in S. oedipus by 4.22%, in S. midas 4.14%, and in L. rosalia only 2.90%.
Tardif et al. (1993) compared the weight development of infants to their adult weight in S. oedipus and C. jacchus. The absolute weight development of the two species was different, but the relative curves of the adult weights were nearly identical. The absolute weight development of the infants in Tardif et al. (1993) is clearly different from our Figure 3. Relative weight development of the studied callitrichids results in this study, in which the curves increase in a shal- to the adult weight of the different species, shown as regression lower line, as depicted in Figure 1a. Furthermore, the au- lines. thors did not report the adult weights as the basis for their computation. If we consult the data on body weights of these species as reported in the literature (e.g., in summary Hershkovitz, 1977, and other sources), then the reports concerning the adult weights in C. jacchus, for instance, range from 240 g to nearly 400 g. When using different adult weights from the same species as base values, the computed relationships of weight development will be correspondingly different as well. Therefore, we compared the weight development of the individuals reported in the present study with the adult weights of these species found at Magdeburg Zoo. The average adult weights of specimens in the Magdeburg Zoo are: C. jacchus – 295 g; S. oedipus – 420 g; S. midas – 480 g; and L. rosalia – 550 g. In this comparison of the weight development in rela- tion to the adult weight, there are no significant differences among the species (Fig. 3).
Present interpretations suggest that the greater the species- Figure 4. Possible dependence of the weight development of specific birth weight, the smaller the weight growth over callitrichids to the birth weight of the respective species. time on a percentage basis, and the longer the time for full 112 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 113
weight development (Fig. 4). This correlation is almost than those of Callithrix. The carrying phase in the onto- linear, and is adequately significant with a correlation coef- genesis of callitrichids is not determined by one single ficient of -0.997. The relationship between the adult weight factor (e.g., body weight or daily path length), but may of a species and the weight development of the infants also have multiple causes. There are also differences in the demonstrates a trend of slower weight development with length of the carrying phase between wild and captive greater adult weight, but this tendency is not definitely individuals. In the zoo setting, for example, some young linear. This trend is considerably less correlated, with a cor- common marmosets are carried up to the age of 18 weeks. relation coefficient of -0.951. In pygmy marmosets (Cebuella pygmaea) this age was 14 weeks (Schröpel, 1988b). Yamamoto (1993) compared data drawn from several studies on the behavioural development of the different Hershkovitz (1977) summarized reports concerning the callitrichid genera. The infants of Callithrix start weaning age of complete adulthood in callitrichids. He indicated from their parents at the age of eight weeks, Saguinus at 18 months for Callithrix and 24 months for both Saguinus 10 weeks, and Leontopithecus at 14 weeks. These observa- and Leontopithecus. These observations are confirmed to tions coincide with the weight development curves we some extent by our results concerning weight development, recorded. Yamamoto (1993) also found a correlation be- although we registered and interpreted the weights only up tween weight and the time when the young are no longer to the 90th day of life. carried on their parent’s back or by another group member. She indicated eight weeks for Callithrix, nine weeks for Of course, hand-rearing is seldom necessary and it will Saguinus, and 12 weeks for Leontopithecus. Tardif et al. therefore require some time to demonstrate or negate (1993), on the other hand, concluded that the duration our results with additional data. Some comparisons of of the carrying phase is not connected with weight devel- published weight curves from other individuals of the spe- opment, but rather with the average species-specific daily cies studied here, or of related species, may only be used path length through their home range. Saguinus groups indirectly, because the methods of rearing are unknown. usually travel daily path distances which are clearly longer Different methods of rearing, and especially the nutrition
Figure 5. Common marmoset, Callithrix jacchus. 16 days old. Figure 6. Cotton-top tamarin, Saguinus oedipus. 19 days old.
Figure 7. Golden-handed tamarin, Saguinus midas. 4 days old. Figure 8. Golden lion tamarin, Leontopithecus rosalia. 22 days old. 114 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 115 of the infants – milk formula, whether the amount of milk is determined by the keeper or by the infant, starting time INTERACCIONES SOCIALES EN UN GRUPO DE of solid food, and so on – may cause different patterns of MONOS AULLADORES ALOUATTA PALLIATA MEXICANA weight development. For example, the curves of weight EN CAUTIVERIO development published by Pook (1978) and Tardif et al. (1993) for Saguinus oedipus increase more slowly than Cristina Domingo-Balcells, Ernesto Rodríguez-Luna ours, but the values found by Rohrhuber (1987) agree Mateo Escobar-Aliaga, Jorge Morales-Mávil with our data. In addition, Tardif et al. (1993) presented weights for Callithrix jacchus which are lower than those Introducción we found. The values published by Kingston (1975) coin- cide with our findings. Son escasos los estudios que abordan las interacciones sociales intragrupales y la jerarquía de dominancia en los Michael Schröpel, Zoologischer Garten Magdeburg, Am monos aulladores de manto Alouatta palliata (Jones, 1980; Vogelgesang 12, D-39124 Magdeburg, Germany. E-mail: Domínguez-Domínguez, 1994; Zucker y Clarke, 1998).
grantes de su misma clase de sexo y edad (Zucker y Clarke, la dieta del mono aullador (Rodríguez-Luna et al., 2003). 1998). En consecuencia, las predicciones de los modelos de El alimento se suministraba diariamente a las 09:00 h, antes competición intragrupal se han de tomar con precaución de lo cual se retiraba el alimento sobrante del día anterior. La para A. palliata y el estudio social ha de ser conveniente- fruta cultivada se situaba en cuatro comederos equidistantes mente contextualizado. y las ramas frescas de árboles silvestres se situaron en una posición central, formando una cama de follaje, por donde En este trabajo se controló la disponibilidad de los recursos podían desplazarse los animales y realizar el forrajeo. para un grupo de monos aulladores, potenciando el compo- nente de competición directa por la acumulación de fruta Inmediatamente después de la captura los animales fueron en comederos. Las condiciones de cautiverio permitieron sometidos a las condiciones de cautiverio del estudio. El la observación directa de las interacciones afiliativas y ag- grupo demoró ocho días en empezar a consumir el ali- onísticas y su direccionalidad en cada díada. Se determinó mento novedoso (fruta cultivada). Tras este periodo todos la jerarquía de dominancia del grupo y se analizaron las in- los individuos se alimentaron de la fruta situada en los teracciones sociales entre sus miembros. Se evaluó también comederos y aceptaron la presencia del observador en el la relación de asociación entre los individuos del grupo y el interior del encierro sin alterar aparentemente su conducta. método para su determinación. El muestreo sistemático inició el ocho de abril de 2002 y se registraron un total de 180 horas de observación repartidas Metodología en 36 días de muestreo, en sesiones de mañana y tarde, de cinco horas cada una. El horario de muestreo abarcaba de Sujetos, lugar de estudio y colecta de datos 09:00 a 14:00 h para las sesiones de mañana y de 14:00 a El grupo de estudio constó de un macho adulto (MA), un 19:00 h para las de tarde. Se utilizó el método de muestreo macho subadulto (MSA), una hembra adulta (HA), una focal-animal (Altmann, 1974; Martin y Bateson, 1991), hembra adulta-vieja (HA+), una hembra juvenil de más muestreando cada individuo durante media hora. Se regis- edad (HJ+) y una hembra juvenil de menos edad (HJ). La tró cada individuo en orden rotatorio en cada sesión, para edad aproximada de los individuos se determinó en fun- balancear los efectos de horario. Se registraron todos los ción de la dentición. Todos los individuos formaban parte eventos de agonismo (mordida, empujón, desplazamiento, de un grupo socialmente establecido en libertad, aunque amenaza) y afiliación (juego, caricia, acicalamiento, abrazo), se desconocía su historia de formación y parentesco entre según la definición dada en el etograma de la especie de sus miembros. El grupo se capturó el 25 de marzo de 2002 Carrera-Sánchez (1993), en los cuales estaba involucrado en Cascajal del Río (Acayucan, Veracruz, México), dentro el animal-focal. del marco de un programa de translocación de esta especie realizado por el Parque de Flora y Fauna Silvestre Tropical Complementariamente al registro focal-animal, cada cinco (PAFFASIT) y auspiciado por la Universidad Veracruzana minutos se realizó un muestreo instantáneo (Altmann, (Xalapa, Veracruz, México). 1974; Martin y Bateson, 1991), en el que se anotaron los individuos que se encontraban en las cercanías del animal- El estudio se realizó en instalaciones del PAFFASIT, focal. Se registraba el nombre del individuo, la actividad localizadas en la Reserva de la Biosfera de Los Tuxtlas, en que realizaba y la distancia al animal-focal medida como: el municipio de Catemaco, Veracruz. El encierro consta de contacto (contacto corporal entre el animal-focal y otro in- una base de hormigón de forma rectangular con diez jaulas dividuo), 1 brazo (distancia no superior a un brazo de mono de 2x3 m, paredes de malla metálica y techo de lámina de aullador de longitud) y 2 brazos (distancia entre uno y dos zinc. Para permitir la exposición de los animales al sol, brazos de longitud). Los individuos que se hallaban a mayor se anexó una jaula de igual tamaño, pero sin cubierta de distancia no se registraban como animales cercanos, ya que lámina. Todas las jaulas están interconectadas por puertas en esa situación la interacción directa entre los individuos y troncos lisos para facilitar la locomoción de los animales. es difícil. El empleo de indicadores de distancia basados en Los troncos conforman un entramado permanente en el in- la longitud del brazo de los monos aulladores permite medir terior de todo el habitáculo a una altura aproximada de un mediante una extrapolación sencilla la distancia, incluso metro y medio desde el suelo, para que los animales puedan cuando el observador está lejos de los animales. Se prefirió desplazarse y descansar. El aprovisionamiento de alimento este método a la medición de proximidad en metros usada constaba de fruta cultivada (melón, papaya, piña y plátano) en otros estudios (por ejemplo, < 1 m para Alouatta palliata y de alimento silvestre colectado diariamente (ramas frescas en libertad [Zucker y Clarke, 1998]; < 5 m para Cercocebus con y sin frutos) de distintas especies reportadas dentro de torquatus [Range y Noë, 2002]).
Tabla 1. Número de agresiones emitidas por cada individuo y su tasa (número de agresiones por hora observación del individuo). Se presenta el total del grupo y la media junto a la desviación estándar. MA = macho adulto, MSA = macho subadulto, HA = hembra adulta, HJ+ = hembra juvenil de más edad, HA+ = hembra adulta-vieja, HJ = hembra juvenil de menos edad. MA MSA HA HJ+ HA+ HJ Total Media SD N° agresiones 17 34 7 25 9 0 92 15.33 12.56 Tasa agresión 0.64 1.23 0.26 0.91 0.34 0 0.564 0.563 0.45 116 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 117
Análisis de datos donde n es el número de individuos y Si la suma de los Se calculó la tasa de agonismo como el número de valores de la fila correspondiente a cada individuo en la eventos agonísticos emitidos por hora de observación tabla de dominancia (Tabla 3). El coeficiente de Kendall del individuo y del grupo. Se realizaron sociogramas en se calcula: K = 1 - d / max d, donde d es el número de 2 función del número y dirección de las interacciones so- tríadas circulares: d = n(n - 1)(2n - 1)/12-1/2 ∑(Si) , y ciales ocurridas durante el estudio para cada díada (pareja donde max d es el número de tríadas circulares máximo de individuos). para un tamaño de grupo determinado. En nuestro estudio, con un número par de individuos (n = 6), la fórmula es: La jerarquía de dominancia del grupo se determinó en max d = 1/24 (n3 - 4n). Presentamos ambos índices pese a función de la dirección de los eventos agonísticos entre que se prefiereh para un número par de individuos, debido los individuos siguiendo el método de Landau (Landau, a que hay subestimación del número de posibles tríadas 1951). A partir del número de eventos emitidos y recibidos circulares y resulta en K < h. por cada individuo, se realizó una matriz de dominancia, donde las filas corresponden al emisor de la agresión y las Además, calculamos los índices de linealidad mejorados por columnas al receptor. La dominancia se establece en fun- De Vries (1995), que evitan sesgos cuando hay díadas bidi- ción de la direccionalidad de la agresión bastando un solo reccionales (nuestro caso). El índice mejorado h’ se calcula: evento de agresión en la dirección A-B para determinar que h’ = h + 6/n3- n * u, donde u es el número de relaciones A domina a B. A esta dominancia se le da un valor de 1. desconocidas. El coeficiente de Kendall mejorado se obtiene Si A nunca domina a B se da el valor de 0 y si entre A y B substituyendo d por d’, siendo d’ = d - 0.25. hay bidireccionalidad se le da valor de 0.5 (Appleby, 1983). Siguiendo esto se genera una matriz de direccionalidad. La La asociación entre los miembros del grupo suele inferirse suma de los valores de dominancia de cada individuo da el a partir de datos de proximidad relativa, usada como in- rango jerárquico, cuanto mayor es el valor mayor rango de dicador (Crockett y Eisenberg, 1987). En nuestro estudio dominancia presenta el individuo en el grupo. valoramos la proximidad en función de tres parámetros: contacto corporal, distancia de un brazo de longitud y dis- Para calcular la linealidad de la jerarquía se aplicó el índice tancia de dos brazos de longitud. Para decidir cual de ellos de Landau h (Landau, 1951) y el coeficiente de Kendall era el mejor indicador de asociación se calculó el índice K (Kendall, 1962). El índice de Landau se obtiene con de diversidad de Shannon-Wiener (H), que determinó 3 2 la siguiente ecuación: h = 12/(n - n) ∑ [Si-1/2 (n - 1)] , la selectividad en cuanto a las parejas potenciales con las que un individuo podía hallarse en proximidad. El índice Tabla 2. Matriz de interacciones agonísticas entre díadas. En las se presenta en función de la diversidad máxima, que de- filas el individuo emisor, en las columnas el individuo receptor. pende del número de individuos del grupo y estandariza MA = macho adulto, MSA = macho subadulto, HA = hembra los resultados para poder compararlos con otros estudios adulta, HJ+ = hembra juvenil de más edad, HA+ = hembra adulta- vieja, HJ = hembra juvenil de menos edad. (Range y Noë, 2002). Una vez decidido el indicador de proximidad más selectivo se calcularon los índices de MA MSA HA HJ+ HA+ HJ asociación diádicos (Lehner, 1979; Martin y Bateson, MA 2 7 1 5 2 1991) con la fórmula TAB / (TA + TB + TAB), donde TAB MSA 0 8 3 16 7 es el tiempo en que los individuos A y B se encontraron HA 0 0 3 2 2 en proximidad selectiva del tiempo de observación de A HJ+ 0 0 8 1 16 sin B, de B sin A y de A con B. Se representó un socio- HA+ 0 0 0 5 4 grama de asociación y se calculó la correlación de Spear- HJ 0 0 0 0 0 man entre el número de afiliaciones entre los miembros de cada díada (en ambas direcciones) y su índice de asoci- ación basado en proximidad. Tabla 3. Matriz de direccionalidad de las interacciones agonísticas. Ver texto para mayor explicación. Rango = rango Resultados de dominancia en función de la suma, en este caso no existen empates en el rango. La matriz se ha ordenado de manera que Las tasas individuales de agonismo fueron bajas (inter- bajo la diagonal queden el mayor número de ceros. MA = macho valo 0 - 1.23), con una tasa media para el grupo de 0.56 adulto, MSA = macho subadulto, HA = hembra adulta, HJ+ = hembra juvenil de más edad, HA+ = hembra adulta-vieja, HJ = (Tabla 1). La mayor parte de interacciones agonísticas hembra juvenil de menos edad. entre los individuos del grupo ocurrieron en un contexto MA MSA HA HJ+ HA+ HJ Suma Rango de alimentación, particularmente relacionadas con los co- mederos donde se presentaba la fruta cultivada. Durante la MA 1 1 1 1 1 5 1 alimentación se produjeron el 75% de los eventos agonísti- MSA 0 1 1 1 1 4 2 cos (53.26% durante la alimentación de fruta y 22.83% HA 0 0 0.5 1 1 2.5 3 durante la alimentación de hojas silvestres), el 17% durante HJ+ 0 0 0.5 0.5 1 2 4 periodos de descanso y el 7% en relación con episodios de HA+ 0 0 0 0.5 1 1.5 5 juego. El tipo de interacción afiliativa más común fue el HJ 0 0 0 0 0 0 6 juego (73.03%); el abrazo representó el 6.96% de las inter- 116 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 117
acciones afiliativas, así como la caricia (6.96%) y el acicala- hembra más joven HJ, existiendo elevada asociación entre miento sólo se presentó el 2.61% de las ocasiones. No hubo los tres miembros más jóvenes del grupo (Figura 2). diferencias significativas entre mañana y tarde en cuanto a interacciones afiliativas o agonísticas. El sociograma de interacciones afiliativas (excluyendo el juego), muestra que MSA fue el más activo, emitiendo La Tabla 2 presenta la matriz de agonismo y la Tabla 3 la matriz de direccionalidad asociada, a partir de la cual se calculó la linealidad de la jerarquía de dominancia. Los resultados fueron los siguientes: h = 0.914, p = 0.044 y h’ = 0.971, p’ = 0.032 (índice de linealidad de Landau y mejorado de De Vries) y K = 0.906, p < 0.05, K’ = 0.937, p’ < 0.05 (coeficiente de Kendall y mejorado de De Vries). Según Martin y Bateson (1991) y Lehner (1979), se con- sidera lineal una jerarquía con índice de Landau superior a 0.9, por lo que encontramos que la jerarquía de dominancia en nuestro grupo de estudio es lineal: MA > MSA > HA > HJ+ > HA+ > HJ (Tabla 3).
Se suele considerar separadamente el rango para hembras y machos, ya que las hembras compiten básicamente por el alimento, mientras que los machos compiten además por el derecho de apareamiento (Van Hooff y Van Schaik, 1992). Por este motivo calculamos también los índices de lineali- dad sólo para las hembras. El resultado fue poco lineal: h = Figura 1. Sociograma de interacciones agonísticas en el grupo. 0.70, p > 0.05 y h’ = 0.90, p’ > 0.05, K = 0.625, p > 0.05 y K’ El macho dominante y la hembra de más alto rango se han representado como alpha. En dirección contraria a las agujas = 0.75, p’ > 0.05. La hembra más joven y pequeña se halla al del reloj, comenzando por la hembra alpha se han ordenado las final de la jerarquía, pero las otras tres hembras forman una hembras por rango jerárquico. Las flechas parten del individuo tríada circular con reversiones agonísticas (Figura 1). Los emisor de la agresión y la punta llega al receptor de la misma. machos al dominar a todas las hembras son los que interac- El grosor de la flecha es proporcional al número de eventos cionaron agresivamente con más individuos. El macho sub- agonísticos entre los miembros de la díada y el número indica el número total de eventos. En negro se presentan las interacciones adulto es el que emitió más conductas agonísticas, seguido agonísticas emitidas por los machos y en gris las de hembras. En por la hembra joven de más edad. La hembra más joven HJ línea discontínua se presentan las reversiones en las agresiones, en es la que recibió mayor número de agresiones, principal- contra del rango jerárquico obtenido. La tríada circular HA, HJ+, mente de HJ+, y nunca emitió agresión hacia ningún otro HA+, se presenta en la esquina inferior izquierda. Ver texto para individuo (Figura 1). El macho dominante interaccionó mayor explicación. preferentemente con la hembra alpha, que fue objeto del mayor número de sus acciones agonísticas y afiliativas (ex- ceptuando el juego) (Figuras 1 y 3).
El análisis de las distancias interindividuales demostró que cuando dos individuos se hallaban en descanso toleraban mayor contacto corporal (21.07% del tiempo), mientras que cuando ambos se alimentaban estaban en contacto únicamente el 0.94%. El 47.86% del tiempo en que los individuos se hallaban descansando se encontraban a una distancia de un brazo y el 30.73% a dos brazos. La distancia durante la alimentación fue de uno y dos brazos de longitud (45.79% en cada caso).
El índice de diversidad para los parámetros de proximidad registrados arrojó que el contacto corporal era el mejor índice de asociación por la elevada selectividad que los indi- Figura 2. Sociograma de asociación entre individuos. El macho viduos mostraban en su permanencia en contacto con otros dominante y la hembra de más alto rango se han representado individuos (Tabla 4). El macho alpha y la hembra alpha como alpha. En dirección contraria a las agujas del reloj, estaban altamente asociados. La hembra alpha, además, se comenzando por la hembra alpha se han ordenado las hembras por hallaba asociada a la hembra vieja HA+ y la hembra joven rango jerárquico. El grosor de las líneas es proporcional al valor del índice de asociación en las díadas (ver texto). El macho alpha sólo de más edad HJ+, de forma que los miembros de la tríada se halla altamente asociado con la hembra alpha. Existe elevada circular presentan altos índices de asociación entre ellas. asociación entre la tríada circular. Las asociaciones entre hembras El macho subadulto pasó más tiempo en contacto con la se han marcado en gris. 118 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 119
afiliación hacia todos los demás individuos, incluso hacia el Alouatta palliata en un estudio durante cuatro años en macho alpha, siendo la afiliación muy recíproca entre ellos. Costa Rica (tasa media 0.38, intervalo anual 0.24 - 0.51). El macho alpha emitió afiliación preferentemente hacia la Esto puede ser debido a que: a) el estudio de Costa Rica hembra alpha, la cual emitió y recibió afiliación recíproca- sólo consideraba a las hembras del grupo y, como muestra mente con la HA+, y recibió el máximo de afiliación de HJ+ este estudio, son los machos los que interaccionan más y MSA (Figura 3). agonísticamente (Figura 1), b) las condiciones de cautive- rio aumentan la tasa agonística por constricción espacial, El cálculo de la correlación de Spearman entre el índice de c) registrar en condiciones de libertad subestima la tasa real asociación y el número de afiliaciones de cada díada (en por la dificultad de registrar todos los eventos, d) el compo- ambas direcciones), indicó que ambos parámetros estaban nente de competición directa (contest competition) fue supe-
correlacionados positivamente (rs = 0.602, p < 0.02, n = rior en nuestro estudio debido a la forma de administrar el 15). Es decir, que los individuos que permanecían más alimento de forma agregada (fruta cultivada en comederos). tiempo en contacto eran los que interaccionaban más afili- Adicionalmente, en Costa Rica se manejaron tasas anuales ativamente. La correlación es negativa, pero no significativa, sin diferenciar estacionalidad en la agregación y disponibi-
entre emisión y recepción de afiliación (rs = 0.48, p > 0.05). lidad de los recursos. Tampoco hubo correlación significativa entre el rango del individuo y la cantidad de afiliación emitida o recibida, ni Probablemente, la plasticidad conductual de esta especie con la emisión o recepción de agresión. también incluye variaciones estacionales en los compo- nentes de competición intragrupal relacionados con la Discusión disponibilidad de alimento en el entorno. La competición directa mediante agresión debe variar con la dinámica La tasa de agonismo media del grupo de estudio (0.56) fenológica de las especies vegetales presentes en el ámbito fue mayor a la reportada por Zucker y Clarke (1998) para hogareño del grupo, al igual que varían los patrones de actividad, forrajeo y distribución espacial en relación con el alimento, especialmente los frutos (Rodríguez-Luna, 2000; Rodríguez-Luna et al., 2003; Serio-Silva, 1992), ya que, a pesar de ser ampliamente generalistas y folívoros, los monos aulladores son selectivos en su elección del alimento (Milton, 1980). Apoyando este razonamiento, observamos que el mayor número de eventos agonísticos tuvieron lugar durante la alimentación, principalmente en relación con los comederos donde se concentraba la fruta.
Wrangham (1980) y Van Schaik (1989) predijeron jerar- quías de dominancia para hembras de primates según el tipo de competición intragrupal. Para los monos aulladores las jerarquías serían poco lineales, aunque consideraron a A. palliata como un caso particular. Zucker y Clarke (1998) reportaron una jerarquía dinámica a lo largo de cuatro años para las hembras, sin correlación rango-edad, pero con una tendencia a que las hembras dominantes sean las jóvenes Figura 3. Sociograma de afiliación entre individuos. El macho recién inmigradas. Sus datos apoyan parcialmente las pre- dominante y la hembra de más alto rango se han representado dicciones de los modelos sociales de Wrangham (1980) y como alpha. En dirección contraria a las agujas del reloj, comenzando por la hembra alpha se han ordenado las hembras Van Schaik (1989), ya que en ciertos momentos la jerarquía por rango jerárquico. El grosor de las líneas es proporcional al es poco lineal, pero existen periodos donde existe estabilidad número de interacciones afiliativas. y linealidad en la jerarquía de dominancia de las hembras.
Tabla 4. Índice de diversidad de Shannon-Wiener para la proximidad con otros individuos medida como contacto, distancia de uno o dos brazos. Se presenta el valor estandarizado como la proporción entre el índice H y la diversidad máxima para un grupo de tamaño seis. También se muestra la media y su desviación estándar. El índice varía entre 0 = máxima selección de pareja y 1 = máxima diversidad. * = Valores inferiores a 0.4, que fueron considerados selectivos. MA = macho adulto, MSA = macho subadulto, HA = hembra adulta, HJ+ = hembra juvenil de más edad, HA+ = hembra adulta-vieja, HJ = hembra juvenil de menos edad. H/Hmax MA MSA HA HJ+ HA+ HJ Media SD Contacto 0.23* 0.38* 0.33* 0.37* 0.39* 0.26* 0.33* 0.656 1 Brazo 0.47 0.38* 0.48 0.46 0.46 0.48 0.45 0.039 2 Brazos 0.48 0.48 0.47 0.47 0.45 0.48 0.47 0.013 118 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 119
Para nuestro grupo de estudio, considerando machos y hem- perceptivas-motoras, que son necesarias para su futuro bras, la jerarquía fue altamente lineal, situando a los machos ajuste y sobrevivencia en el entorno del bosque tropical, dominando sobre las hembras y básicamente los individuos sino que también aprenden el comportamiento social adultos sobre los no-adultos. La jerarquía entre hembras fue complejo que caracteriza su vida en grupos compactos poco lineal debido a una tríada circular formada por las dos (Crockett y Eisenberg, 1987). hembras adultas y la juvenil de más edad, próxima a la mad- urez sexual. Las reversiones en la dominancia entre las hem- La hembra joven de mayor edad (HJ+) fue también muy bras podrían ser consecuencia de las características de los activa socialmente, pero interactuando de distinta forma miembros del grupo, principalmente edad, madurez sexual que el macho subadulto. HJ+ presentó la segunda mayor e historia de formación del grupo en cuanto a migraciones tasa de agonismo (tras MSA), siendo el principal recipiente y parentesco. Por tanto, la conducta social intragrupal debe de sus agresiones la hembra más joven de menor rango. ser convenientemente contextualizada para poder interpre- La presencia de reversiones en la jerarquía donde estaba tar las interacciones entre los individuos de los grupos y sus involucrada HJ+ indica la inconsistencia de la domi- relaciones de asociación y dominio. nancia entre las hembras de mono aullador predicha en los modelos sociales de Wrangham (1980) y Van Schaik El patrón de migración de los aulladores resultaría en grupos (1989), y a su vez apoyan la hipótesis de que HJ+ se hal- con adultos no emparentados. La jerarquía de dominancia laba en el proceso de aumentar de rango en su grupo natal, reportada muestra una tendencia a que los inmigrantes lo que se vería favorecido posiblemente por la avanzada recientes dominen sobre los más viejos residentes (Jones, edad de las dos hembras adultas. Ambos factores no son 1980; Zucker y Clarke, 1998). La jerarquía de dominancia contradictorios, pero sin más datos no es posible dar una de nuestro grupo de estudio posiblemente variaría en un es- explicación totalmente satisfactoria para la tríada circular tudio a más largo plazo, debido a que en cautiverio no sería del grupo de estudio. posible la migración de los individuos jóvenes MSA y HJ+. Es posible que se establecieran nuevos individuos alpha con La mejor medida de asociación en función de distancias un aumento de agonismo durante el periodo intermedio, interindividuales para monos aulladores en condiciones consecuencia del balance de fuerzas entre los individuos de cautiverio, se debe calcular con base en el tiempo en alpha y los jóvenes adultos. De hecho, durante el estudio que dos individuos permanecen en contacto corporal, por estos individuos ya estaban presentando las mayores tasas ser el indicador de proximidad más selectivo. Es necesario de agonismo. establecer previamente el mejor indicador de asociación por proximidad en cada caso particular y no usar dis- En cuanto a la afiliación, la conducta afiliativa de acicala- tancias arbitrarias que quizás no aporten la información miento, tan importante entre monos del Viejo Mundo requerida. El índice de asociación tuvo una correlación (Jones, 1980; Neville et al., 1988), fue un evento poco positiva con el número de interacciones afiliativas en las común entre aulladores (2.61% de las afiliaciones en el díadas, esto último además aporta direccionalidad, por grupo). Incluso en una especie del mismo género como lo que se sugiere una combinación de ambos parámetros A. seniculus, el acicalamiento es más común que en A. palliata, para el establecimiento de relaciones entre los miembros lo cual puede tener que ver con las diferencias entre ambas de los grupos. especies en cuanto a patrones de competición entre hem- bras, ya que las de A. palliata no forman alianzas por paren- En nuestro estudio, los individuos que permanecían más tesco en los grupos (Sánchez-Villagra et al., 1998). tiempo en contacto eran los que interaccionaban más afili- ativamente. Esto no fue consecuencia de la mayor proximi- El juego fue la conducta afiliativa más importante, con dad entre ellos, como muestra el caso de HJ+ y HA+, donde más del 70% del tiempo dedicado a interacciones afili- la elevada cercanía entre ellas no se correspondía con un ativas en el grupo. En nuestro estudio el individuo social- gran número de interacciones afiliativas (Figuras 2 y 3). El mente más activo fue el macho subadulto, emitiendo afili- registro de proximidad no fue direccional por la imposibi- ación y agresión hacia el resto de individuos en la mayor lidad de registrar el responsable de la misma en todos los proporción. Nunca se registró agresión de este macho casos. Inferimos que el responsable de la proximidad en hacia el macho alpha, pero sí un elevado porcentaje de las díadas correspondería al emisor del mayor número de afiliaciones, incluyendo el juego. Todos los individuos del afiliaciones en cada díada. Por ejemplo, la responsable de grupo participaron activamente en los episodios de juego, la proximidad entre HA y HJ+ podría ser HJ+, ya que es a veces colectivamente. Durante el desarrollo de los aul- ésta la que emite el grueso de las interacciones afiliativas en ladores, la cantidad de tiempo invertido, la intensidad y esa díada. La responsabilidad entre HA y HA+ sería más la complejidad del juego varía, pero se considera que tiene recíproca (Figuras 2 y 3). La elevada asociación entre HJ+ un lugar predominante en su historia vital (Carpenter, y HA+ no sería debida a una asociación real entre ellas, 1965). Junto con el macho joven, las dos hembras jóvenes sino sería una consecuencia indirecta de la asociación de participaron en el juego en la mayor proporción, lo que ambas con la tercera hembra (con la hembra alpha HA). En demuestra la importancia social de este tipo de afiliación otras palabras HJ+ y HA+ se hallan en contacto corporal durante el desarrollo y vida social de los monos aulladores. a menudo no porque exista un vínculo intenso entre ellas Jugando no sólo practican activamente las capacidades sino porque ambas “quieren estar con la HA”. En cuanto a 120 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 121 los machos, el macho alpha sólo presenta elevado número emos al personal del PAFFASIT su trabajo de manten- de afiliación con la hembra alpha y esto coincide con el imiento de las instalaciones de cautiverio y aprovision- mayor tiempo que pasan en contacto, pero no presenta amiento de los animales. Y a la Dra. Liliana Cortés y la elevada asociación con las hembras HJ+ y HA+, por lo que Dra. Mariella Superina por sus comentarios en la revisión se deduce que cuando se acerca el macho a la hembra alpha de este artículo. las otras se alejan. Cristina Domingo-Balcells, Ernesto Rodríguez-Luna, La composición del grupo de estudio en cuanto a clases de Mateo Escobar-Aliaga y Jorge Morales-Mávil, Instituto de sexo-edad y el análisis de las interacciones sociales y distan- Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, cias interindividuales, nos hacen plantearnos los siguientes México. E-mail:
Martin, P. y Bateson, P. 1991. La Medición del Comportamiento. Alianza Editorial, Madrid. NEWS Milton, K. 1980. The Foraging Strategy of Howler Monkeys. A Study in Primate Economics. Columbia University Press, Washington, DC. A POSSIBLE FIELD SIGHTING OF CALLICEBUS Milton, K. 1998. Physiological ecology of howlers BERNHARDI IN NORTHERN MATO GROSSO (Alouatta): Energetic and digestive considerations and During a birdwatch- comparison with the Colobinae. Int. J. Primatol. 19: ing trip to the Alta 513-548. Floresta area of Mato Neville, M. K., Glander, K. E., Braza, F. y Rylands, A. Grosso, Brazil, in Oc- B. 1988. The howling monkeys, genus Alouatta. En: tober 2003, our small Ecology and Behavior of Neotropical Primates, Vol. 2, R. A. group (myself, a fellow Mittermeier, A. B. Rylands, A. F. Coimbra-Filho y G. A. traveler and our guide) sighted two titi monkeys B. da Fonseca (eds.), pp.349-453. World Wildlife Fund, which looked very much like Callicebus bernhardi. Washington, DC. They had very black faces with red beards, gray Range, F. y Nöe, R. 2002. Familiarity and dominance above their eyes, gray hands and feet, and a gray tail relations among female sooty mangabeys in the Taï with a white tip. We were able to see the monkeys National Park. Am. J. Primatol. 56: 137-153. clearly through binoculars, but none of us had a Rodríguez-Luna, E. 2000. Cambios en la estrategia de camera along. forrajeo del mono aullador (Alouatta palliata mexicana): Estudio de una población en un fragmento de selva. Tesis We made the sighting in a 50 ha reserve adjoining the Flo- de maestría, Instituto de Neuroetología, Universidad resta Amazonica Hotel in Alta Floresta, about five minutes Veracruzana, Veracruz. from the airport. We were birding along a dirt road which Rodríguez-Luna, E., Domínguez-Domínguez, L. E., runs parallel to the property, and sighted the monkeys at Morales-Mávil, J. E. y Martínez-Morales, M. 2003. the edge of the reserve forest. The area around the reserve is Foraging strategy changes in an Alouatta palliata developed with housing. mexicana troop released on an island. En: Primates in Fragments: Ecology and Conservation, L. K. Marsh (ed.), Doug Trent, our guide, has worked in Brazil for over 20 pp.229-250. Kluwer Academic / Plenum Publishers, years, and had the chart of titi monkeys from Van Roos- New York. malen et al. (2002). We compared the monkeys that we had Sánchez-Villagra, M. R., Pope, T. R. y Salas, V. 1998. seen to the chart, and Callicebus bernhardi was the only one Relation of intergroup variation in allogrooming to group which looked like them. Doug Trent knew that C. bernhardi social structure and ectoparasite loads in red howlers had not been reported from the Alta Floresta area. The (Alouatta seniculus). Int. J. Primatol. 19: 473-491. owner of the hotel, Vitoria da Riva Carvalho – who is also Serio Silva, J. C. 1992. Patrón diario de actividades y the director of the reserve – told us that she knew there were hábitos alimenticios de Alouatta palliata en semilibertad. titis in the reserve, but not which species. Further surveys of Tesis de licenciatura, Facultad de Biología, Zona Córdoba, the fauna there are needed. Universidad Veracruzana, Veracruz. Van Hooff, J. A. R. A. M. y Van Schaik, C. P. 1992. Carole Stepp, 10363 Glenbarr Avenue, Los Angeles, CA Cooperation in competition: The ecology of primate 90064, USA. E-mail: <[email protected]>. Doug Trent bonds. En: Coalitions and Alliances in Humans and may be contacted at
pasarían a ser parte de la Zona de Amortiguamiento de las tres áreas naturales protegidas. Dichas etnias tendrán una participación decisiva a través de los comités de gestión de cada una de las áreas naturales protegidas mencionadas. Estas tres áreas se localizan en medio de un macizo aislado de la cordillera de los Andes, en medio de los ríos Apurímac, Ene, Tambo y Urubamba.
Cabe destacar que la acción del gobierno y de las comuni- dades indígenas, así como de organizaciones conservacio- nistas nacionales e internacionales, ha sido un proceso muy antiguo, que viene desde la década de los 60 y que hoy día se plasma con la formalización de estas áreas. Por otro lado, asegurar la conservación de esta importante área significa Figure 1. The Black Lion Tamarin Ecological Station, Pontal do una continua planificación del territorio con un enfoque de Paranapanema, São Paulo, Brazil. Corredor de Conservación, que combina los mecanismos de conservación de las propias comunidades y la participación Diabo State Park – the Ecological Station provides perma- de las diferentes instituciones en el desarrollo sostenible, nent protection for four important populations of the spe- combinando las actividades económicas sostenibles con la cies: in the Fazendas Tucano and Rosanella, Fazenda Santa conservación de la biodiversidad. Mônica, Fazenda Ponte Branca, and Fazenda Santa Maria. The estimated total population is over thirty animals. IPÊ La Zona Reservada Apurimac está ubicada en una cordillera – Instituto de Pesquisas Ecológicas drew up the original escabrosa e inaccesible con varias montañas que superan los proposal and supported the Instituto Brasileiro do Meio 4000 msnm y todavía contiene restos de los grandes bosques Ambiente e dos Recursos Naturais Renováveis (IBAMA) de montaña que antiguamente cubrían gran parte de los and the Ministry of the Environment in its creation. The Andes tropicales orientales, de Venezuela a Bolivia (Boyle, challenge now is to implement the reserve, and plans are 2001). Los bosques supervivientes del Apurimac contienen underway for reforestation to join the forest patches and una notable biodiversidad que incluye varias especies raras extend a corridor to the main population of L. chrysopygus y endémicas, pero esta región aislada ha permanecido casi in the Morro do Diabo State Park. inexplorada por biólogos. Esta área es especialmente inte- resante en lo que respecta a la biogeografía de primates, ya Cláudio Valladares-Pádua, IPÊ – Instituto de Pesquisas que la cresta de Vilcabamba está ubicada en cercanías de la Ecológicas, Caixa Postal 47, 12960-000 Nazaré Paulista, zona de contacto de las áreas de distribución de distintos São Paulo, Brazil. E-mail:
TRES NUEVAS ÁREAS NATURALES PROTEGIDAS Tres expediciones han realizado observaciones en esta área EN PERÚ en los años 1997 y 1998, dos del Programa de Evaluación Rápida (Rapid Assessment Program, RAP) de Conserva- Tres nuevas Áreas Naturales Protegidas en la cordillera de tion International y uno del Programa el Hombre y la Bio- Vilcabamba, para el SINANPE, es el resultado de la catego- sfera (Man and the Biosphere Program, MAB) de la Smith- rización de la Zona Reservada Apurimac: Reserva Comunal sonian Institution. Estas expediciones han cooperado para Ashaninka, Parque Nacional Otishi y Reserva Comunal documentar la excepcional riqueza biológica de la región, Matziguenka, de acuerdo al Decreto Supremo 003-2003- y su informe final realizado en conjunto incluyó una pro- AG publicado el 15 de enero, 2003 en el Diario Oficial El puesta para crear un Parque Nacional y Reservas Comuna- Peruano. Esta región tiene particular importancia por la les (Alonso et al., 2001). Entre muchos otros hallazgos que presencia de varias especies de primates, y el esfuerzo que resultaron de estas expediciones, se descubrió a Cuscomys se hizo para declarar las áreas protegidas fue apoyada por ashaninka, un nuevo género y una nueva especie de roedor grupos de investigadores de Conservation International. perteneciente a la familia de los Abrocomidae (Emmons, 1999). Adicionalmente, los equipos del RAP confirmaron Del total de 1,669,200 ha que tenía la Zona Reservada la presencia de varios grandes primates en el área, los cuales Apurimac, 709,347.06 ha se destinan a la creación de están sufriendo una seria presión cinegética en altitudes tres áreas naturales protegidas: Parque Nacional Otishi más bajas. Observaciones en el sitio más alto evaluado en con 305,973.05 ha, Reserva Comunal Ashaninka con el RAP, a 3500 msnm, no produjeron evidencias de pri- 184,468.38 ha y Reserva Comunal Matziguenka con mates; pero en el segundo sitio más alto se hallaron varias 218,905.63 ha. La diferencia del total de lo que era la Zona especies que ocupaban una franja de bosque inusual en la Reservada del Apurímac se constituye en comunidades nati- base de una pared alta, aproximadamente a 2500 msnm. vas tituladas, Ashaninkas y Matziguenkas, cuyos territorios Aquí, el equipo observó Cebus apella y posiblemente 122 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 123
C. albifrons, y registró vocalizaciones de Ateles chamek y de international conservation organizations, has been an ongo- monos nocturnos (probablemente Aotus nigriceps). ing process which was begun in the 1960s, and which has culminated in the legal protection of these areas. Ensuring En el tercer sitio, sólo 1000 m más alto que el Río Urubam- the conservation of this important region, however, will ba, los equipos hallaron Aotus, Lagothrix lagothricha, Cebus require a continuing planning process for the territory with apella y C. albifrons y oyeron vocalizaciones de Alouatta se- a focus on implementing a conservation corridor, which niculus y Ateles chamek. Algunas de estas especies (Alouatta, combines the conservation mechanisms of the communities Ateles, Lagothrix y C. albifrons) fueron halladas por Edmund and the participation of different institutions in sustainable Heller en el año 1915, junto con Saimiri boliviensis y Sa- development, which combines sustainable economic activi- guinus fuscicollis weddelli. Aunque su distribución sugeriría ties with the conservation of biodiversity. su presencia en la región, no se registró ningún ejemplar de Pithecia por ninguno de los equipos de biodiversidad y los The new protected areas cover the highest portions of a pobladores locales no incluyeron a este género en una lista rugged and inaccessible mountain range, often rising above de primates conocidos (Rodríguez y Amanzo, 2001). No se 4000 m, which still harbors remnants of the great montane espera que Callicebus, Callimico y Cebuella estén presentes forests which once covered much of the eastern tropical en esta área. Andes from Venezuela to Bolivia (Boyle, 2001). The surviv- ing forests of the Apurimac hold remarkable biodiversity, Estas y otras expediciones científicas más recientes han do- including many rare and endemic species, but this isolated cumentado otras especies importantes de vertebrados, entre region has been largely unexplored by biologists. It is espe- ellas el “hormiguero gigante” (Myrmecophaga tridactyla), cially interesting in terms of primate biogeography, as the el “oso de anteojos” (Tremarctos ornatus), el “gallito de las Vilcabamba ridge lies near the meeting of species bound- rocas” (Rupicola peruviana) y el “caimán blanco”(Caiman aries for several primate genera, including Pithecia mona- crocodylus). Además, se encuentra una rica diversidad de chus and P. irrorata, Saguinus fuscicollis weddelli and S. f. flora como el “ulcumano o romerillo” Podocarpus( sp.), el leucogenys, and two taxa of Lagothrix. “quinual” (Polylepis sp.) y el “cedro de altura” (Cedrela sp.), entre otras. Three expeditions surveyed this area in 1997 and 1998, two from the Rapid Assessment Program (RAP) of Con- Para acceso a imágenes y entrevistas por favor contacte a servation International and one from the Man and the Nina Pardo,
These and other recent scientific expeditions have et al., 2001; see also Gärdenfors, 2001), and comments also documented many other vertebrate species in the received on these drafts were used to improve and refine new protected areas, including giant anteater (Myr- the guidelines. mecophaga tridactyla), spectacled bear (Tremarctos orna- tus), Andean cock-of-the-rock (Rupicola peruviana), and The Guidelines for Application of IUCN Red List Criteria at white cayman (Caiman crocodylus). This area is also di- Regional Levels: Version 3.0 have been published as a booklet verse in its flora, which includes the “romerillo” (Podo- in three languages: English, French and Spanish. They are rec- carpus sp.), quinual trees (Polylepis sp.) and cedar trees ommended for anyone who wishes to use the IUCN Red List (Cedrela sp.). Categories and Criteria to undertake Red List assessments at the regional level. They are now available on the SSC website For more information and images of the protected areas, as PDF files, in the three languages, at:
Erick Meneses, Director, Vilcabamba Regional Program, Craig Hilton-Taylor, Red List Programme Officer, Species Conservation International-Peru, Malecón de La Reserva Survival Programme, 219c Huntingdon Road, Cambridge 281, Miraflores - Lima 18, Peru, and John M. Aguiar, CB3 0DL, UK. E-mail:
have resulted in an extraordinary and diversified combina- tion of research, management and education programmes THE ROLE OF PRIMATES AS SEED DISPERSERS IN THE – many of them pioneer – and accompanying, and often VEGETATION STRUCTURE OF TROPICAL FORESTS leading in, the developing science of conservation biology. This meeting was attended by 127 people – a good sample Introduction of the researchers and students (47), conservationists, and managers and staff of protected areas, both foreign and Seed dispersal is an important process affecting the density Brazilian, who are involved directly, and sometimes indi- and distribution of plants and the floristic composition of rectly, with such aspects of conservation as: behavioural, plant communities. Frugivorous species play a key role in the ecological and demographic studies; population genetics natural regeneration mechanism of tropical forests, as 45-95% and management (including translocation and reintro- of tropical plant species depend on animals to disperse their duction programmes); habitat and landscape protection seeds (McKey, 1975; Terborgh, 1983). Primates represent and restoration; captive breeding, management and 25-40% of frugivore biomass in tropical forests, and therefore husbandry; and environmental education and rural exten- as a group they play a very important role in seed dispersal in sion, as well as public policy, institutional development tropical forests (Eisenberg and Thorington, 1973). and capacity-building, and professional training – all elements of the conservation programmes established for At the 10th Brazilian Congress of Primatology, held in the lion tamarin species, Leontopithecus rosalia, L. chrys- November, 2002, at the Federal University of Pará, Belém, omelas, L. chrysopygus and L. caissara. The aim, succesfully Brazil, a roundtable entitled “Seed Dispersal” discussed the achieved, was to discuss, renew and broaden partnerships role of primates as seed dispersers in structuring the vegeta- amongst the numerous students, professionals and profes- tion of Brazilian tropical forests. Participants presented their sional institutions involved in lion tamarin conservation data for different species of primates, covering a number of – reporting on their work, exchanging views on their ex- key aspects of seed dispersal. periences, integrating and planning scientific studies and, most especially, engaging a younger generation of prima- Seed dispersal by Saguinus niger, Cebus apella and tologists who will be responsible for the programmes over Brachyteles arachnoides the coming years. Ana Cristina Oliveira monitored the feeding behavior of a The opening of the meeting was marked by a presenta- group of Saguinus niger for six months in eastern Amazo- tion of the book Lion Tamarins: Biology and Conservation, nia. The diet of the group was predominantly frugivorous: edited by Devra G. Kleiman and Anthony B. Rylands, and 87.5% of recorded feeding behavior was of fruits. Of 16 published in 2002 by the Smithsonian Institution Press. species of plants providing fruits, Saguinus ingested and Afterwards, in a moment of reflection, Cláudio Valladares- defecated whole seeds from at least six. Seeds with diameter Pádua then read an homage to José Márcio Ayres, “The >1 cm and/or length >2 cm were discarded. Seeds that were primatologist who liked to create reserves”, who had died ingested took from two to four hours to pass through the at a young age just two months previously, in March, 2003 digestive tract. In association with the movement patterns of (see Neotropical Primates 11(1): 39-41, 2003). Over the fol- the group, 19.3% of the seeds taken from mature forest were lowing two days there were talks and roundtables on the dropped in secondary forest, demonstrating clearly that Sa- following themes: “Leontopithecus as a model for primate guinus niger plays an important role in the dispersal of seeds conservation”, “Current status of the genus Leontopithecus”, from primary forest trees, and contributes to succession in “Processes and tools for the conservation of Leontopithecus”, the secondary forest (Oliveira, 2002). “Conservation of fragmented habitats”, and “Institutional cooperation and its importance in the conservation of the Following a similar line of investigation, the research of Patrí- genus Leontopithecus”, besides three general sessions with cia Izar in the Atlantic Forest of Intervales State Park, São a further 18 talks. The abstracts, published in the Livro de Paulo, analyzed the characteristics of fruiting species exploited Resumos, are listed on page 138 of this issue. by Cebus apella and Brachyteles arachnoides. Her results showed that the quantity of fruits produced affected the seed dispersal Special thanks are extended to the Director and staff of the by both primate species – that is, the greater the production, Serra dos Órgãos National Park, Teresópolis, for their hos- the greater the number of seeds dispersed. Comparing the size pitality and generosity in hosting the meeting. of seeds dispersed by Cebus and Brachyteles, she found that the former was a more efficient disperser of smaller seeds (limited Denise Marçal Rambaldi, Associação Mico-Leão-Dou- by diameter), whereas Brachyteles arachnoides was evidently a rado, Rodovia BR-101, Km 214, Caixa Postal 109.968, more efficient disperser of large seeds (Izar, 2002). Casimiro de Abreu, 28860-970 Rio de Janeiro, Brazil, e-mail:
Itapuã State Park, Rio Grande do Sul. Seeds from their feces In the next stage of her research, Carla Castro will experi- were separated, identified through a seed bank established ment with the seeds found in the marmosets’ feces, as well from a phenological study of 257 trees, shrubs, and lianas as those collected from trees for in vitro germination. This encountered in the study area, and used in germination technique has the advantage of reducing seed infestation by tests. These tests were conducted in a greenhouse, with fungi or other pathogenic agents, since the seeds are washed forest soil in special trays, protected from birds and ants in disinfectant agents, inoculated and maintained under and under daily monitoring for a period of 12 months. controlled temperature and light conditions. The objective of Germination rates of seeds collected from feces (tests) and this technique is the creation of germplasm banks to conserve from ripe fruits (control) were compared using the Chi- the plant species dispersed by this primate (Castro, 2002). square test. Significant differences were found between tests and controls in five of the 10 species tested. For Syagrus The Study of Seed Dispersal: Future Perspectives romanzoffiana, Erythroxylum argentinum and Lithraea brasiliensis, the percentage of ingested seeds that germinated Post-dispersal represents the longest phase of the plant life successfully was higher than that of the control seeds, while cycle, since it involves seed germination, seedling establish- for Enterolobium contortisiliquum and Myrciaria cuspidata, ment and tree maturation (Howe et al., 1985). Few studies the control seeds germinated better than those ingested. have explored this phase, likely due to the difficulty in track- S. romanzoffiana accounted for 24.12% of the total fruit ing the plant’s growth over a long period of development. ingested during the 13 months of the study. These fruits Maria Aparecida Lopes showed that more recent studies are available for almost the whole year, and Alouatta guariba have broadened their approach and are examining all aspects clamitans was evidently an efficient disperser for this species of the dispersal process – from fruit removal to seedling re- in terms of an increase in the number of germinated seeds, cruitment – with new techniques employing stable isotopes their defecation far from the parent tree, and the quantity and genetic markers, which will allow for the identification of seeds ingested (Marques, 2002). of seed and seedling origin (Lopes, 2002). Participants in the roundtable emphasized the importance of preserving Germination In Vivo and In Vitro as Tools to Conserve primate populations as a means of guaranteeing plant diver- the Plant Species Dispersed by Callithrix jacchus in the sity in the Amazon and Atlantic Forests. The use of stable Atlantic Forest isotopes and genetic markers for the identification of seed and seedling origin, as well as in vitro germination, will pro- Carla S. S. de Castro used in vivo germination tests to verify vide important tools in the study of seed dispersal. the viability of seeds dispersed by Callithrix jacchus, and also created a germplasm bank for the species involved. Acknowledgements: We thank the organizing committee and She studied two groups of marmosets for 18 months in an Stephen Ferrari (President) of the Xth Brazilian Congress of Atlantic Forest remnant in the Dunas State Park, in Natal, Primatology. We are also grateful to the Brazilian Science Rio Grande do Norte. Council (CNPq) for financing research on Callithrix jac- chus; the Margot Marsh Biodiversity Foundation and the The marmosets ingested seeds from Coccoloba sp., Campo- Brazilian Higher Education Authority (CAPES) for financ- manesia dichotoma and Hexaclamys itatiaiae. Average lengths ing research on Alouatta guariba clamitans; the São Paulo of the seeds were 5.7 mm, 6.0 mm and 5.6 mm, respectively. State Research Support Foundation (FAPESP – Fundação Seeds were collected from the marmoset feces at average dis- de Amparo à Pesquisa do Estado de São Paulo) for financ- tances of 16.8 m, 60.0 m and 45.3 m, respectively, from the ing research on Cebus apella and Brachyteles arachnoides; parent tree, reflecting the movement patterns of marmoset and the CNPq and the Amazon Environmental Research groups within their home ranges. Seeds from feces (tests) and Institute (IPAM – Instituto de Pesquisas Ambientais da seeds taken from ripe fruits (control) were planted with forest Amazônia) for financing research onSaguinus niger. soil, and kept in a greenhouse (germination in vivo). The percentage of seeds germinating and the time to germination Carla S. S. de Castro, Departamento de Botânica, Ecologia were compared using the Kruskall-Wallis and the Mann- e Zoologia, Universidade Federal do Rio Grande do Norte, Whitney U-tests. For seeds of Coccoloba sp. and Campoma- Avenida Senador Salgado Filho s/n, Campus Universitário, nesia dichotoma, the proportion germinating was greater, and Lagoa Nova, Natal 59078-970, Rio Grande do Norte, Brazil, the time to germination was shorter, in those collected from e-mail:
References Experimental Horco Molle, Tel: (0381) 425-0396, E-mail:
Mariela Nieves, Grupo de Investigación en Biología Evolu- IPS 2004 PRE-CONGRESS WORKSHOP: tiva (GIBE), Departamento de Ecología, Genética y Evolu- “CAPUCHINS: THE STATE OF THE ART” ción, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón II, 4to. A workshop, “Capuchins: The State of the Art,” will be Piso, Laboratorios 46-47, (1428) Buenos Aires, Argentina. held prior to the XXth Congress of the International Pri- E-mail:
Primate Conservation, Incorporated (PCI) is a not-for- Topic 1. Social structure and ecology – Leader discussants: profit foundation established to fund field research that Linda Fedigan (University of Calgary, Alberta, Canada) supports conservation programs for wild populations of and Patrícia Izar (University of São Paulo, São Paulo, primates. Priority will be given to projects that study, in Brazil); Topic 2. Cognition – Leader discussants: Patrizia their natural habitat, the least known and most endangered Potì (Istituto di Scienze e Tecnologie della Cognizione, species. The involvement of citizens from the country in CNR, Rome, Italy) and Katie Leighty (University of which the primates are found will be a plus. The intent is Georgia, Athens, USA); Topic 3. Capuchin Behavioral to provide support for original research that can be used Economics – Leader discussants: Frans de Waal (Emory to formulate and to implement conservation plans for the University, Atlanta, USA) and Camillo Padoa Schioppa species studied. (Harvard Medical School, Boston, USA); Topic 4. Social learning and traditions – Leader discussants: Susan Perry Eligibility: Primate Conservation, Inc. will grant seed (Department of Anthropology, UCLA, Los Angeles, USA monies or provide matching grants for graduate students, and Max Planck Institute for Evolutionary Anthropology, qualified conservationists and primatologists to study Leipzig, Germany) and Elsa Addessi (Istituto di Scienze e rare and endangered primates and their conservation Tecnologie della Cognizione, CNR, Rome, Italy). General in their natural habitat. Grants have averaged approxi- discussion. Looking into the future. In addition to the above mately $2,500, with a maximum grant of $5,000. We themes, the following topics will be addressed in the general do not support conferences, travel to scientific meet- discussion: (a) the new proposed taxonomy for the genus 128 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 129
and its implications for captive management; (b) conserva- tion, human-animal interactions. Fees: We will charge each BECOME A MEMBER OF THE INTERNATIONAL participant 160 Euro (and 110 Euro for students), covering PRIMATOLOGICAL SOCIETY all meals (all lunches and dinner from the 18th to the the 22nd, excluding the dinner in Siena), all coffee breaks, a To become a member of the International Primatological concert, a trip to Siena, transport from Poggibonsi to Radi- Society, please contact Steven J. Schapiro, IPS Treasurer condoli, and the bus trip from Radicondoli to Grosseto and Vice President for Membership, UTMDACC, 650 Railway Station (from where the train for Turin departs). Cool Water Drive, Bastrop, TX 78602, USA, Tel: +1 The fee does not include the train ticket to Grosseto- 512 321 3991, Fax: 512 332 5208, e-mail:
Elisabetta Visalberghi, Istituto di Psicologia, Consiglio Na- The ASP Search Committee selected and the Board of Di- zionale delle Ricerche, Via Aldrovandi 16 B, 00197 Roma, rectors approved the nomination of Linda Fedigan as the Italy. E-mail:
With support from NCRR grant RR 15311, Coordinated but we will not accept renewals unless you wish to pay Information Services for Primate Research, the Wisconsin the (exorbitant) price of $60/year in the U.S. or $80/year Primate Center is engaged in a project to scan key primate outside the U.S. newsletters so that users of PrimateLit can link directly to the full text of articles indexed by the Primate Information And, if you have paid, but are now willing to print your own Center, Seattle. We have approximately ten other primate copies, please let us know and we will send our blessings newsletters that we hope to scan and make accessible and thanks. through the database. PrimateLit already includes links to over 65,000 biomedical articles indexed in the National Judith E. Schrier, Editor, Laboratory Primate Newsletter, Library of Medicine’s PubMed. Within the limitations of Box 1853, Psychology Department, Brown University, copyright, our goal is to make PrimateLit a window to the Providence, RI 02912, USA, e-mail
The second list is LPN-PDF, which sends out the immense PDF file to subscribers. Frankly, we don’t know why anyone would want to get this and clog their mailboxes; but people RECENT PUBLICATIONS do want it, so we provide it.
To subscribe to any of these options, send a message as A MUST-HAVE BOOK FOR PRIMATE-WATCHERS follows: Setchell, J. M. and Curtis, D. J. (eds.). 2003. Field and SUBSCRIBE LPN-L your-own-name Laboratory Methods in Primatology: A Practical Guide. SUBSCRIBE LPN-WARN your-own-name Cambridge University Press, Cambridge, UK. 343 pp. SUBSCRIBE LPN-PDF your-own-name $100.00 (USD). Reviewed by Clara B. Jones. to [email protected]. If this book had been available when I began conducting field studies in 1973, I would have learned fewer lessons All of these lists are used quarterly, since the LPN is by trial and error. Setchell and Curtis, researchers in the a quarterly publication. There may be an occasional early years of their careers, have produced a comprehensive announcement besides, but that has been rare in the past. and knowledgeable volume summarizing many of the most important aspects of primate research. In their words, “If If you have paid for paper issues of the LPN, you will this book proves useful to fieldworkers, acts to stimulate continue to receive them until your subscription runs out, research and understanding of primates in their natural 130 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 131
state, and through that increased knowledge can make mates primarily in their own right, and especially in rela- some small contribution to primate conservation, then tion to humans, rather than as components of communities we will have achieved our aim” (Curtis and Setchell, 2003: and ecosystems governed by “first principles.” Approaches 12). Field and Laboratory Methods in Primatology (hereaf- to the study of animals found in mainstream ecology and ter, FLMP) is likely to accomplish the authors’ objectives. natural history journals (e.g., Ecology, Oikos, Conservation Since their Introduction includes a detailed overview of the Biology, The American Naturalist) are, on the whole, not volume, here I will highlight what seem to me its primary reflected in this volume. If primatologists are to become strengths and weaknesses. integrated with the wider community of natural scientists, it will be necessary for us to adopt standard approaches and It is necessary to reveal a bias borne of age and, perhaps, procedures of population, community and ecosystem ecol- fading memory. Like elders recalled from my own youth, I ogy, not only the science of the individual and his or her note a growing tendency to romanticize my early years in group or population. the field and, armed with anecdote, to exaggerate my past experiences studying monkeys. But I do think it may be Primates are evolved taxa positioned in the dynamic accurate to say that when I began as a fieldworker, research context of abiotic and biotic forces, subject to the same was conducted with fewer ethical constraints – or, rather, constraints governing other taxa, and the present volume with less self-consciousness about these issues. One rarely neither provides such a holistic (ecological) perspective nor hesitated to collect animals, to conduct field manipulations, the insights or procedures required to study the Order with to mark individuals, to place weighty transmitter collars the tools of population, community and ecosystem ecol- around their necks, and otherwise intervene in the natural ogy. The website of the American Society of Mammalo- course of events, as long as this was considered to serve the gists (see
the mammalogist Sydney Anderson. It covers all mammals Ambiental e Conservação. A abordagem participativa na known to occur in the Madidi National Park which weigh educação para a conservação da natureza – S. M. Padua, more than 200 g, including eight primates. The treatment M. F. Tabanez & M. das G. de Souza, pp.557-591; Análise for each species includes an illustration and a distribution da sustentabilidade de caça em florestas tropicais no Peru map, plus notes on identification, body measurements, – Estudo de caso – R. E. Bodmer & J. G. Robinson, pp.593- habitat and habits, and conservation status – and for the 629; Entrevistas e aplicação de questionários em trabalhos terrestrial mammals, a description and illustration of their de conservação – E. M. Ditt, W. Mantovani, C. B. Valla- tracks. Available from: Conservacíon Internacional – Bolivia, dares-Pádua & C. Bassi, pp.631-646; Manejo integrado de Caller M. Pinilla No. 291, Esq. Av. 6 de Agosto, Casilla espécies ameaçadas – C. B. Valladares-Pádua, C. S. Martins 13593, La Paz, Bolivia, Tel: (591-2) 434058 / 435225, e- & R. Rudran, pp.647-665. O livro poderá ser adquirido na: mail:
– B. S. Low; 12. Social monogamy in a human society: (cloth), 0 226 42464 2 (paperback). Price: Cloth - $75.00, Marriage and reproductive success among the Dogon – B. Paper - $30.00. The first systematic attempt to understand I. Strassmann; 13. Social monogamy in gibbons: The male relationships among primate life histories, ecology, and perspective – U. H. Reichard; 14. Pair living and mating social behavior. Topics covered include how primate life strategies in the fat-tailed dwarf lemur (Cheirogaleus histories interact with rates of evolution, predator pres- medius) – J. Fietz; 15. Social monogamy and its variations sure, and diverse social structures; how the slow maturation in callitrichids: Do these relate to the costs of infant care? of primates affects the behavior of both young and adult – Anne W. Goldizen; 16. Monogamy in New World pri- caregivers; and reciprocal relationships between large brains mates: What can patterns of olfactory communication tell and increased social and behavioural complexity. Contents: us? – Eckhard W. Heymann. Available from: Cambridge Foreword – R. D. Martin, xi-xx; Primate life histories and University Press, 40 West 20th Street, New York, NY socioecology – P. M. Kappeler, M. E. Pereira & C. P. van 10011-4221, USA, Fax: +1 212-691-3239. General Address Schaik, pp.1-23. Part 1. Life History and Socioecology. Pri- (Orders, Customer Service): Cambridge University Press, mate life histories and phylogeny – A. Purvis, A. J. Webster, 100 Brook Hill Drive, West Nyack, NY 10994-2133, USA, P.-M. Agapow, K. E. Jones & N. J. B. Isaac, pp.25-40; So- Tel: +1 845-353-7500, Fax: +1 845-353-4141. Website: cioecological correlates of phenotypic plasticity of primate
1-881173-73-9. Conservación Internacional Serie de Guías from the anthropological study of nonhuman primates Tropicales de Campo, edited by Jose Vicente Rodríguez-Ma- to the wider academic and nonacademic world. Avail- hecha. In Spanish. Illustrations by Stephen D. Nash, César able from: Cambridge University Press, 40 West 20th Lanadazábal Mendoza and Margarita Nieto Díaz. This is Street, New York, NY 10011-4211, USA, Tel: (800) 872- a remarkable and amply and beautifully illustrated guide 7423, Fax: (914) 937-4712, e-mail:
Di Fiore, A. 2003. Ranging behavior and foraging ecol- ARTICLES ogy of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuní National Park, Ecuador. Am. J. Pri- Adams, J. S., Chen, H., Chun, R. F., Nguyen, L., Wu, S., matol. 59(2): 47-66. Ren, S. Y., Barsony, J. and Gacad, M. A. 2003. Novel Dominy, N. J., Svenning, J. C. and Li, W. H. 2003. Histor- regulators of vitamin D action and metabolism: Lessons ical contingency in the evolution of primate color vision. learned at the Los Angeles Zoo. J. Cell. Biochem. 88(2): J. Hum. Evol. 44(1): 25-45. 308-314. Dominy, N. J., Garber, P. A., Bicca-Marques, J. C. and Aze- Ascunce, M. S., Oklander, L. and Mudry, M. D. 2003. vedo-Lopes, M. A. de O. 2003. Do female tamarins use Amplification of mitochondrial COII gene from DNA visual cues to detect fruit rewards more successfully than extracted from hair samples in some species of New do males? Anim. Behav. 66: 829-838. World monkeys. Folia Primatol. 74(3): 165-167. Duarte-Quiroga, A. and Estrada, A. 2003. Primates as pets Ascunce, M. S., Cortés-Ortiz, L. and Mudry, M. D. 2003. in Mexico City: An assessment of the species involved, The mitochondrial control region of the black howler source of origin, and general aspects of treatment. Am. J. monkey, Alouatta caraya (Primates, Platyrrhini), and the Primatol. 61: 53-60. development of new primers. Molec. Ecol. Notes 3(3): Fioravanti, C. 2003. Macacos quase falantes. Pesquisa, Ciên- 372-375. cia e Tecnologia no Brasil 85: 34-39. Fundação de Amparo Ascunce, M. S., Hasson, E. and Mudry, M. D. 2003. COII: à Pesquisa do Estado de São Paulo (FAPESP), São Paulo. A useful tool for inferring phylogenetic relationships March 2003. Website:
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Brito, B., Brandão, R. A. & Rocha, S. B. Áreas protegidas ABSTRACTS para os micos-leões, p.30. Câmara, I. de G. Leontopithecus como modelo para a con- Selected abstracts from the Primate Society of Great Brit- servação de primatas tropicais em unidades de conserva- ain Spring Meeting, School of Psychology, University of ção, p.18. St. Andrews, Fife, Scotland, 10-11 April, 2003. In: Pri- Cardos, B. M. S. Experiências do Zoo de Salvador em mate Eye 80, June 2003. reprodução de Leontopithecus chrysomelas (Kuhl, 1820) (Callitrichidae, Primates), p.61. Ashley, P. J., Neill, J. C., Middelmiss, D. N. and Hendrie, Coelho, A. S., Ruiz-Miranda, C. R. & Kleiman, D. G. C. A. Behavioural and physiological methods for the as- Ontogenia dos choros e trinos emitidos por micos-leões- sessment of social status in pair housed common marmo- dourados, Leontopithecus rosalia, p.57. sets (Callithrix jacchus), p.3. Coimbra-Filho, A. F. Desafios do passado e presente na Barrett, L. From ‘what now?’ to ‘what if?’: Quotidian cogni- conservação dos micos-leões, p.17. tion and cognitive control, pp.3-4. Cullen Jr., L. Agrofloresta, eco-negociação e a conservação da Blackwood, N., Pearce, P., Scott, L. and De Ruiter, J. Do biodiversidade no Pontal do Paranapanema, São Paulo, p.37. age and sex affect responsiveness to novelty in common Dietz, J. D., Ballou, J. & Baker, A. J. Conseqüências gené- marmosets? p.5. ticas e demográficas da fragmentação das populações de Buchanan-Smith, H. M., Smith, A. C., Surridge, A. K., micos-leões, p.33. Prescott, M. J., Osorio, D. and Mundy, N. I. Colour Deitz, L. A. A contribuição das ONGs, p.44. vision and cognition in primates, pp.5-6. Eloy, E. C. C., Oliveira, M. M., Laroque, P. & Porfírio, S. A Caldwell, C. and Whiten, A. Can scroungers be learners? aplicação da experiência com micos-leões no manejo das Social learning in common marmosets, Callithrix jacchus, populações cativas de primatas brasileiros, p.62. p.6. Fandi, A. C., Santos, G. R. dos & Gomes, A. R. Educação Laland, K. Necessity is the mother of primate invention: ambiental para a sustentabilidade do entorno da Reserva An examination of behavioural innovation in primates, Biológica de Una (REBIO Una), p.55. pp.9-10. Fernandes, R. V. & Rambaldi, D. M. Corredores florestais: Moura, A. C. de A. and Lee, P. C. The cognitive abilities of Novos caminhos para o mico-leão-dourado, p.38. Cebus apella libidinosus: Tool use and survival in a harsh Grativol, A. D., Fernandez, F. & Cooper, A. DNA antigo environment, p.12. e genética da conservação do mico-leão-dourado (Leonto- Snowdon, C. T. Social learning in cooperative breeders, pithecus rosalia), p.56. pp.16-17. Henry, M. D., Bales, K. L., Miller, K. E. & Dietz, J. D. Valero, A. and Byrne, R. W. Do spider monkeys have Effects of resource availability on reproductive patterns in mental maps? A new procedure to study animal move- golden lion tamarins (Leontopithecus rosalia), p.66. ments in the wild, p.24. Kierulff, M. C. M. & Procópio de Oliveira, P. Programa Van Bergen, Y., Almond, R. and Brown, G. R. Marmosets de translocação de micos-leões-dourados (Leontopithecus go back to school: The role of food sharing in learning rosalia), p.29. about food, pp.17-18. Lapenta, M. J., Procópio de Oliveira, P. & Kierulff, M. C. M. O mico-leão-dourado (Leontopithecus rosalia) como In: Livro de Resumos: III Simpósio sobre Micos-Leões, dispersor de sementes na Reserva Biológica União / Parque Nacional da Serra dos Órgãos, Teresópolis, Rio IBAMA, Rio das Ostras – RJ, p.52. de Janeiro, Brasil, 26-28 de maio de 2003. Centro de Martins, C. S. & Valladares-Pádua, C. B. Atual status da Proteção de Primatas Brasileiros, Cabedelo, Paraíba, As- conservação de Leontopithecus chrysopygus, p.22. sociação Mico-Leão-Dourado, Casimiro de Abreu, Rio Matsuo, P. M. & Boucinha, V. Envolvendo escolas na de Janeiro. conservação do mico-leão-dourado e da mata Atlântica, p.54. Amaral, A. T., Prado, F. & Valladares-Pádua, C. B. Es- Monteiro, R. V. & Jansen, A. M. Doenças em primatas e o timativa do tamanho populacional de micos-leões-de- risco da fragmentação dos ambientes naturais, p.36. cara-preta (Leontopithecus caissara) na Ilha de Superagüi, Nascimento, M. T. Estrutura da vegetação em habitats Guaraqueçaba, PR, Brasil, p.64. fragmentados, p.35. Bampi, M. I. Cooperação institucional e sua importância Oliveira, M. M. de. A contribuição do Centro de Proteção na conservação de primatas do gênero Leontopithecus: “A de Primatas Brasileiros no esforço de conservação dos contribuição do IBAMA”, p.41. micos-leões, p.42. Beck, B. B., Castro, I., Martins, A., Rambaldi, D., Dietz, J. Paranhos, K. M., Martins, C. S. & Valladares-Pádua, C. B. D., Kleiman, D. G. & Rettberg-Beck, B. Causes of loss Resultados preliminares da atualização do status popula- of reintroduced golden lion tamarins and their offspring, cional do mico-leão-preto, Leontopithecus chrysopygus, no p.28. Parque Estadual Morro do Diabo, SP, p.63. Bento, M. I. da S. & Santos, M. B. Ações integradas para o Paschoal, F. R. Contribuição dos zoológicos brasileiros na desenvolvimento sustentável dos assentamentos no entor- conservação do gênero Leontopithecus, p.45. no da Reserva Biológica Poço das Antas / IBAMA, p.53. Passos, F. C. A contribuição das universidades, p.43. 138 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 139
Pissinatti, A. A contribuição das populações em cativeiro, Brumm, H. & Todt, H. Acoustic communication in noise: p.27. Regulation of signal characteristics in primates and birds, Prado, F., Valladares-Pádua, C. B. & Amaral, A. T. Levanta- p.82. mento populacional de mico-leão-de-cara-preta (Leonto- Buchanan-Smith, H. & Prescott, M. Inter-specific social pithecus caissara) no estado de São Paulo, Brasil, p.65. learning in mixed species troops of tamarins, p.43. Procópio de Oliveira, P. Atual status da conservação do Buchanan-Smith, H., Smith, A., Surridge, A., Prescott, gênero Leontopithecus “Mico-leão-dourado (Leontopithe- M., Osorio, D. & Mundy, N. Colour vision in primates: cus rosalia)”, p.21. Effects on foraging behaviour, efficiency and learning Procópio de Oliveira, P., Veruli, V. P. & Keirulff, M. C. M. abilities, p.82. Estrutura do habitat na Reserva Biológica União, p.51. Caldwell, C. A. & Whiten, C. A. Can scroungers be learn- Raboy, B. E. GHLTs: Proactive conservation for the 21st ers? Social learning in the common marmoset, Callithrix century, p.23. jacchus, p.227. Rambaldi, D. M. & Godoy, F. Sequestro de carbono: De la Torre, S. & Snowdon, C. T. Babbling in wild pygmy Novas oportunidades para a mata Atlântica e os micos- marmosets, pp.88-89. leões, p.49. Fernández-Duque, E. & Rotundo, M. Are female owl mon- Rapaport, L. & Tressoldi, B. A inflûencia do forrageamento keys imposing social monogamy on males, p.92. social no desenvolvimento dos micos-leões-dourados sel- Falótico, T., Verderane, M. P., Resende, B. D., Ottoni, E. B. vagens, p.59. & Izar, P. Rank reversal in females’ hierarchy in semi-free- Ruiz-Miranda, C. R., Morais, M. M. de, Martins, A. & ranging capuchin monkeys (Cebus apella), p.158. Beck, B. B. Conservação dos micos-leões em fragmentos Fujita, K., Kuroshima, H. & Masuda, T. Spontaneous de- de mata: Espécies invasoras, condição física dos animais e ception by capuchin monkeys (Cebus apella) in an experi- comportamento social, p.34. mental food-competition contest? p.58. Ruiz-Miranda, C. R., Amorim, A. P. S., Beck, B. B., Bonad- Garber, P. A., Bicca-Marques, J. C. & Azevedo-Lopes, iman, S. F. & Martins, A. Diferenças de peso entre micos- M. A. de O. Experimental field study of decision- leões-dourados (Leontopithecus rosalia) reintroduzidos making in two species of wild tamarins: Changing nascidos em cativeiro e sua prole sob diferentes manejos foraging strategies under conditions of changing food pós solta, p.58. availability, p.44. Silva, B. A., Guedes, P. G., Boubli, J. P. & Salles, L. O. Giménez, M. C. & Fernández-Duque, E. Summer and Descrição preliminar das estruturas microscópicas dos winter diet of night monkeys in the gallery and thorn pelos-guarda de Leontopithecus rosalia (Linnaeus, 1766) forests of the Argentinean chaco, p.164. e Leontopithecus chrysomelas (Kuhl, 1820) (Platyrrhini, Juarez, C. P., Rotundo, M. & Fernández-Duque, E. Behav- Primates), p.60. ioral sex differences in the socially monogamous night Valladares-Pádua, C. B. José Márcio Ayres, o primatologo monkeys of the Argentinean chaco, p.174. que gostava de criar reservas, pp.5-6. (Obituary.) Kleiman, D. G. & Ruiz-Miranda, C. R. Behavioral compe- Venorin, L. B., Godoy, F. & Fernandes, R. V. Mapeamento tencies and reintroduction of captive-bred animals, p.11. de RPPNs como instrumento de conservação do habitat Lefebvre, L. & Sol, D. Innovation and learning vary with para o mico-leão-dourado, p.50. seasonality and food distribution, p.48. Lefebvre, L., Bouchard, J. & Reader, S. Social learning in Selected abstracts from the 28th International Ethological mammals and birds: Similarities and differences, p.37. Conference, Florianópolis, Santa Catarina, Brazil, 20-27 Lopes Araújo, F., Lopes, N. A., Santos, B. L. and Yama- August, 2003. In: Revista de Etologia, 5 (Suppl.), 2003. moto, M. E. Influence of the number of food sources C. R. Ruiz-Miranda, M. J. R. Paranhos da Costa, R. H. on feeding competition in captive Callithrix jacchus, Macedo, A. V. Peretti and C. Ades (eds.). p.178. Odália-Rímoli, A. Development of socialization of muriqui Almond, R. E., Van Bergen, Y. & Brown, G. R. Marmosets infants (Brachyteles arachnoides), p. 189. go back to school: The role of food sharing in the devel- Oliveira, D. A. G. & Ades, C. Form and function in the opment of infant food preferences, p.73. roars of two howler monkey species, p.189. Baldovino, M. C. Infant handling in tufted capuchin mon- Rapaport, L. & Tressoldi, B. Social foraging in immature keys (Cebus apella), p.143. golden lion tamarins (Leontopithecus rosalia) in the União Bezerra, B. M., Schiel, N., Souto, A. & Huber, L. The Federal Biological Reserve, RJ, Brazil, p.197. development of saltatory search in Callithrix jacchus (Pri- Resende, B. D., Izar, P. and Ottoni, E. B. Interaction be- mates: Callitrichidae), p.79. tween social play and nutcracking behavior in semifree Bicca-Marques, J. C., Garber, P. A. & Azevedo-Lopes, M. tufted capuchin monkeys (Cebus apella), pp.198-199. A. de O. An experimental study of social foraging in wild Ruiz-Miranda, C. R. Behavioral aspects of habitat fragmen- titi monkeys (Callicebus cupreus) under conditions of tation, p.18. changing patch quality, p.35. Stamps, J. A. Habitat selection: Animal behavior meets Bonnie, K. E. & de Waal, F. B. M. Monkey see, monkey landscape ecology, pp.13-14. do? Factors affecting observational learning in brown Santos, L. R. & Hauser, M. D. The cotton-top tamarin’s capuchin monkeys (Cebus apella), p.80. understanding of tools, p.44. 140 Neotropical Primates 11(2), August 2003 Neotropical Primates 11(2), August 2003 141
Schiel, N. & Huber, L. The ontogeny of social learning in tackling the on-going global biodiversity crisis. Organized free-living Callithrix jacchus, p.45. by Alexandra Zimmermann (North of England Zoologi- Slater, P. J. B., Deecke, V. B. & Rainey, H. J. Calls and alarm cal Society), Chris West (Zoological Society of London), calls: Some problems of predator recognition, p.70. Matthew Hatchwell (Wildlife Conservation Society) and Snowdon, C. T. Cooperative learning in cooperative breed- Richard Lattis (Wildlife Conservation Society). For further ers, p.45. details contact: Alexandra Zimmermann, NEZS Conserva- Souto, A. & Moonen, C. How Callithrix jacchus and Cal- tion Coordinator, at
Pursuit of Ecological Sustainability”. The aim is to focus at- tion and conservation sites in and near New York City have tention on, and to advance the understanding of, issues sur- been organized to highlight the possibilities that exist. For rounding the pursuit of ecologically sustainable use and the more information, please visit the meeting website at
IV Congresso Brasileiro de Unidades de Conservação, Association of Tropical Biology and Conservation – 2005 17 a 21 de outubro de 2004, Curitiba, Paraná, Estação Annual Meeting, 23-29 July, 2005, Uberlândia, Brazil. Embratel 21 Convention Center. Realização: Rede The venue will be the Uberlândia Convention Center. For Nacional Pró-Unidades de Conservação e Fundação O more information write to the Chair of the Organizing Boticário de Proteção à Natureza, Rua Gonçalves Dias 225, Committeee, Kleber del-Claro, Laboratório de Ecologia Curitiba 80240-340, Paraná, Brasil. Website:
ERRATUM In the note cited below, the correct unit of measurement for morphometric characters should be millimeters (mm) not centimeters (cm). The author apologizes for any confusion or inconvenience this error may have caused the reader. None of the results or conclusions is changed due to this oversight.
Jones, C. B. 2003. Chest circumference differs by habitat in Costa Rican mantled howler monkeys: Implications for resource allocation and conservation. Neotrop. Primates 11(1): 22-24. 142 Neotropical Primates 11(2), August 2003
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Submissions Journal article Stallings, J. D. and Mittermeier, R. A. 1983. The black-tailed Please send all English and Portuguese contributions to: marmoset (Callithrix argentata melanura) recorded from Paraguay. John M. Aguiar, Conservation International, Center for Applied Am. J. Primatol. 4: 159–163. Biodiversity Science, 1919 M St. NW, Suite 600, Washington, DC 20036, Tel: 202 912-1000, Fax: 202 912-0772, e-mail: Chapter in book
Short articles. These are usually reviewed only by the editors. A broader range of topics is encouraged, including such as Printed on New Leaf Reincarnation Matte 80# cover (100% recycled/50% post- behavioral research, in the interests of informing on general consumer waste, processed chlorine free) and New Leaf Reincarnation Matte 70# research activities which contribute to our understanding of text (50% recycled/30% post-consumer waste, elemental chlorine free). By using this environmentally friendly paper, Conservation International saved the following resources: platyrrhines. We encourage reports on projects and conservation 6 fully-grown trees and research programs (who, what, where, when, why, etc.) and 621 gallons of water most particularly information on geographical distributions, 4 million BTUs of energy 294 pounds of solid waste locality records, and protected areas and the primates which 357 pounds of greenhouse gases occur in them. Texts should not exceed 10 pages in length Calculated based on research done by Environmental Defense and other members of the Paper Task Force. (1.5 spaced, including the references). For more information about New Leaf Paper, go to www.newleafpaper.com.
Neotropical Primates A Journal and Newsletter of the IUCN/SSC Primate Specialist Group Vol. 11(2), August 2003
Contents Short Articles
Environmental Education: A Teaching Tool for the Conservation of Pygmy Marmosets (Cebuella pygmaea) in the Ecuadorian Amazon Stella de la Torre and Pablo Yépez...... 73 The Discovery of a New Population of Black Lion Tamarins (Leontopithecus chrysopygus) in the Serra de Paranapiacaba, São Paulo, Brazil Fabio Röhe, André Pinassi Antunes and Cristina Farah de Tófoli ...... 75 On the Occurrence of the Black Lion Tamarin (Leontopithecus chrysopygus) in Buri, São Paulo, Brazil Fernando Silva Lima, Izabel Cristina da Silva, Cristiana Saddy Martins and Cláudio Valladares-Pádua ...... 76 Dieta, Área de Vida, Vocalizações e Estimativas Populacionais de Alouatta guariba em Um Remanescente Florestal no Norte do Estado do Paraná Lucas de Moraes Aguiar, Nélio Roberto dos Reis, Gabriela Ludwig e Vlamir José Rocha...... 78 Callithrix geoffroyi (Primates: Callitrichidae) and Alouatta caraya (Primates: Atelidae) in the Serra do Cipó National Park, Minas Gerais, Brazil Leonardo de Carvalho Oliveira, Edeltrudes Maria V. C. Câmara, André Hirsch, Ana Maria Oliveira Paschoal, Rodrigo Martins Alvarenga and Maycon G. Belarmino...... 86 Distribuição do Guigó (Callicebus coimbrai) no Estado de Sergipe Marcelo Cardoso de Sousa ...... 89 Estimativa de Densidade e Tamanho Populacional de Sauá (Callicebus nigrifrons) em Um Fragmento de Mata em Regeneração, Viçosa, Minas Gerais, Brasil Regiane C. Romanini de Oliveira, Andressa Sales Coelho e Fabiano R. de Melo...... 91 Primates of Brownsberg Natuurpark, Suriname, with Particular Attention to the Pitheciins Marilyn A. Norconk, Mary Ann Raghanti, Sara K. Martin, Brian W. Grafton, L. Tremaine Gregory and Bart P. E. De Dijn...... 94 Primates in a Forest Fragment in Eastern Amazonia Oswaldo de Carvalho Jr...... 100 Some Observations on the Predation of Small Mammals by Tufted Capuchin Monkeys (Cebus apella) Briseida D. Resende, Vivian L. G. Greco, Eduardo B. Ottoni and Patrícia Izar...... 103 Insect-eating by Spider Monkeys Andres Link...... 104 Lagothrix lagothricha or Lagothrix lagotricha: Which is it? Thomas R. Defler ...... 107 Births of Alouatta caraya and A. belzebul (Atelidae, Alouattinae) in Captivity in Brazil Daniela Fichtner Gomes and Júlio César Bicca-Marques...... 109 Weight Development of Hand-Reared Callitrichids Michael Schröpel ...... 110 Interacciones Sociales en Un Grupo de Monos Aulladores Alouatta palliata mexicana en Cautiverio Cristina Domingo-Balcells, Ernesto Rodríguez-Luna, Mateo Escobar-Aliaga y Jorge Morales-Mávil ...... 114
News...... 121
Primate Societies ...... 128
Recent Publications ...... 130
Meetings...... 140